Journal of
Veterinary Medicine and Animal Health

  • Abbreviation: J. Vet. Med. Anim. Health
  • Language: English
  • ISSN: 2141-2529
  • DOI: 10.5897/JVMAH
  • Start Year: 2009
  • Published Articles: 350

Full Length Research Paper

Comparative cost analysis of three injectable ivermectin preparations in the control of gastrointestinal nematodes of sheep in Makurdi, Benue State Nigeria

Mathew Adamu
  • Mathew Adamu
  • Department of Veterinary Parasitology and Entomology, College of Veterinary Medicine University of Agriculture Makurdi Nigeria.
  • Google Scholar
Paul Amuta
  • Paul Amuta
  • Department of Animal Health and Production, College of Veterinary Medicine, University of Agriculture Makurdi Nigeria.
  • Google Scholar
Anthony Ameh
  • Anthony Ameh
  • Department of Veterinary Parasitology and Entomology, College of Veterinary Medicine University of Agriculture Makurdi Nigeria.
  • Google Scholar
Samuel Ode
  • Samuel Ode
  • Department of Veterinary Pathology, College of Veterinary Medicine, University of Agriculture Makurdi Nigeria.
  • Google Scholar


  •  Received: 10 September 2018
  •  Accepted: 27 December 2018
  •  Published: 28 February 2019

 ABSTRACT

The efficacy and comparative cost analysis of three injectable ivermectin preparations was evaluated in West African Dwarf (WAD) sheep naturally infected with gastrointestinal nematodes. Three anthelmintics: ivomec classic® (IVC), ivomec super® (IVS) and ivomec gold® (IVG) were administered at a dose rate of 200µg/kg to control gastrointestinal nematodes in three treatment groups comprising five animals each. The faecal egg counts (FEC) for each animal pre-treatment, and thereafter for a period of 16 weeks post-treatment was carried out using the modified McMaster technique. The results is a pre-treatment mean FEC for groups A, B and C of 970±550.36, 880± 279.55 and 1640±893.78 eggs per gram (epg), respectively and a mean FEC of zero for all treatment groups one week post treatment. The mean FEC of zero was maintained for 28, 35 and 56 days, respectively. A mean FEC threshold for re-treatment of 500 epg was exceeded at days 42, 49 and 84 for groups A (615±167.26), B (830±287.49) and C (737.5±448.10), respectively. The results were subjected into a deterministic model to estimate the costs of using IVC, IVS or IVG in an annual control program. The costs of a one-time treatment were $20.6, $20.8 and $21.0, respectively. The average annual costs were $82.39, $83.22 and $41.99 for groups A, B and C, respectively. Thus, veterinary service and labour are two variables that contributed more to cost of treatment when compared with the price of drugs and average weight of the animals treated.

Key words: Ivermectin, gastrointestinal nematodes, West African Dwarf sheep, efficacy, cost analysis.

 


 INTRODUCTION

Gastrointestinal (GI) parasite  infection  is  considered  as the  most  important limiting factor to sheep productivity in most parts of the world especially in developing countries (Waller, 1997; Roeber et al., 2013; Blackie, 2014; Singh et al., 2017a, b). The most common GI parasitic diseases in sheep in Nigeria are Haemonchosis, Strongyloidosis, Oesophagostomosis, Bunostomosis and Trichostrongylosis.

Haemonchus contortus has been singled out as the most important nematode of small ruminants in the tropics (Adamu et al., 2013; Singh et al., 2013; Zvinorova et al., 2016). Gastrointestinal nematode infections poses serious economic consequences to small ruminant production due to the associated morbidity, mortality, veterinary service and cost of treatment, as well as costs of other control measures (Singla, 1995; Zinsstag et al., 1998; Nwosu et al., 2007).

In ruminant production systems, parasite control has consistently shown a very high correlation with increased production (Kumar et al., 2013; Kenyon et al., 2013). Gastrointestinal nematode control strategies are almost entirely on the use of anthelmintic. The frequent use and mismanagement of these drugs has led to development of wide-spread resistance to the major groups of anthelmintic except for monepantel (Pomroy, 2006; Molento, 2009; Adamu et al., 2013; Melaku et al., 2013).

Ivermectin (IVM) is a  macrocyclic lactone with activity against GI and lung nematodes (Nolan, 2012; Campbell, 2012), as well as against ectoparasites of clinical relevance in domestic animals (Campbell et al., 1984; Shoop et al., 1995; Merola and Eubig, 2012). Ivermectin has extensive tissue distribution, low biotransformation and high plasma-GI recycling that guarantees its persistent activity. The broad spectrum of activity and wide margin of safety has made it a drug of choice for nematode and arthropod parasitism in cattle, sheep, goat, swine, dog and horses (Campbell et al., 1983). Consequently, IVM is the most widely used anthelmintic and this extensive use has led to the emergence of IVM-resistant nematode populations in several countries (Jackson and Coop, 2000; Waller, 2006; Pomroy, 2006; Molento, 2009). The efficacy of IVM against gastrointestinal parasites under different control strategies has been demonstrated (Kenyon et al., 2013).

Farmers and veterinarians should be interested in information concerning the cost analysis of using different drugs and strategies to help with decision making for better control options. The decision making process is dependent on the costs of the anthelmintic, veterinary service and labour. These three variables may change depending on cost of anthelmintic, efficacy and duration of action against GI nematodes.

Currently, there are three injectable IVM preparations in the market produced by Merial. These IVM preparations are ivomec classic®, ivomec super® and ivomec gold®. The preparations differ in composition, duration of action and price. The aim of this study was to determine the efficacy, duration of action and cost implications of these IVM preparations as demonstrated by faecal egg counts pre and post-treatment for a period of 16 weeks in a flock of sheep.

 


 MATERIALS AND METHODS

Experimental animals and ivermectin preparations

A total of fifteen West African Dwarf sheep kept at the University Teaching and Research Farm, University of Agriculture, Makurdi were randomly selected for this experiment. The sheep included 7 rams and 8 ewes out of a herd of 35 sheep. The sheep were kept under the semi-intensive system of management. Pregnant ewes and lambs were excluded from this experiment.

The compositions of the three injectable IVM preparations used in this experiment were: Ivomec classic® (IVC) contains 1% m/v of ivermectin; Ivomec super® (IVS) contains 1% m/v of ivermectin and 10% clorsulon and Ivomec gold® (IVG) contains 3.15% m/v of ivermectin. All three formulations used were manufactured by Merial South Africa (Pty) Limited. The anthelmintic was administered at a dose rate of 200 μg of IVM per kilogram body weight according to manufacturer’s instructions.

Experimental design

The fifteen sheep were randomly assigned to 3 treatment groups (A, B and C), with each group comprising 5 sheep. Sheep in group A were treated with IVC, while sheep in groups B and C were treated with IVS and IVG, respectively.

Prior to the administration of the IVM preparations, a baseline faecal examination was carried out to determine the faecal egg counts of individual sheep pre-treatment. The sheep were weighed individually using a Camry® weighing scale.

The months of August to October represent the second half of the rainy season including its peak. During this period, it is expected that Haemonchus L3 are well established in grazing pasture to pose a sufficient challenge to the experimental animals. The IVM formulations were administered to the sheep in the different groups at the same dose rate of 200 µg/kg subcutaneously, as recommended by the manufacturer.

Sampling and determination of faecal egg counts

Following treatments, faecal samples were collected per rectum from all the sheep in each group once weekly for 16 weeks. Samples were placed in polythene bags, labeled and transported on ice packs to the laboratory for further processing and examination.

The faecal samples were examined for helminth eggs and the faecal egg counts (FEC) for each sample was determined using the Modified McMaster technique using saturated sodium chloride solution as the floatation medium (Hansen and Perry, 1990).

Data collection and analysis

Prior to treatment with the respective injectable IVM preparations, the FEC for each of the 5 sheep per group was examined and recorded. The mean and standard error of the mean (SEM) were calculated and recorded for each group. The FEC of each sheep in the three groups was determined once weekly for a duration of 16 weeks. The mean FEC for each group and the SEM was similarly calculated for each group weekly. The FEC of 500 epg was used as the cut-off value in this study for a repeat of treatment (the week in which the mean FEC exceeded 500 epg was referred to as “re-treatment week”). The time interval between the week of first treatment  and the re-treatment week was regarded as the “duration of action” of the drug and it was noted for each group.

Economic analysis

A deterministic economic model was developed using Microsoft Excel to demonstrate the cost implications of using each of the IVM formulations with i representing the treatment groups (IVC, IVS and IVG). Table 2 shows the input values for variables used to develop the model. The calculated variables include: drug price per ml (dpi), average weight of sheep in each group (AWi), average dosage administered per group (DAi), average cost of drug per treatment per group (Dci), veterinary service cost per group (VSci), labour cost per treatment per group (Lci), duration (weeks) till next treatment for each IVM preparation (DTi) and number of treatments required per year (NTi). The outcome of these calculations is the average annual cost of GI nematode control per group (ATCi). VVci means veterinary visit cost.

Economic model calculations

Dci was calculated for each group by multiplying DAi with dpi as follows:

The average cost of a one-time treatment per group (Tci) is the sum of veterinary visit cost (VVci); and Dci, VSci and Lci for five sheep as follows:

The NTi was determined based on the fact that the rainy season provides an environment conducive for the proliferation of GI nematodes on pasture. The rainy season usually lasts about 6 months (24 weeks) during which several life-cycles of the parasites are expected to occur. Therefore, NTi differed between groups based on their respective DAi as follows:

              

The average annual cost of GI parasite control for one group (ATci) is the product of the Tci and the NTi of the respective group.

Sensitivity analysis

A sensitivity analysis was conducted in order to determine the level of impact of some variables on the annual cost of GI parasite control for each drug. This was done by adjusting the input values of certain variables by ±20% one at a time, while all other variables remained constant at their default values. The resulting average annual cost of GI parasite control (ATci) from each simulated scenario was compared with the default ATci calculated from the values from the field experiment. Variables for which sensitivity analysis was done include: veterinary visit cost (VVci), veterinary service cost (VSci), labour cost (Lci), the price of the drugs (DPi) and the average weight of the animals (AWi).

 


 RESULTS

The mean faecal egg count for the three groups of 5 sheep treated with the three different ivermectin preparations are illustrated in Figure 1. The pre-treatment mean FEC across the groups is as follows: 970 epg for group A, 880 epg for group B and 1640 epg for group C (Table 1). One week after treatment, all the animals in the three groups presented 0 epg on examination of faecal samples. This is indicative of the efficacy of all three IVM preparations 7 days post treatment as 100%.

 

 

 

The three IVM formulations delayed re-infection for different durations. Sheep in group A treated with IVC maintained 0 epg status until day 28 post treatment, sheep in group B treated with IVS maintained 0 epg status until day 35 post treatment and sheep in group C treated with IVG maintained 0 epg status until day 56 post treatment. This implied that following clearance of infection, IVC, IVS and IVG prevented patent infection for a period of 28, 35 and 56 days, respectively.

Garg et al. (2007)reported a mean FEC of 500 epg in sheep requires anthelmintic treatment. The results in Table 1 therefore indicate the need for re-treatment on day 42 following treatment using IVC, day 49 following treatment with IVS and day 84 following treatment with IVG. The period of importance for the control of H. contortus is the rainy season which lasts about 6 months (180 days) on average in the study area. This implies the use  of  IVC  and  IVS  will  require 4 treatments per year, while farmers that use IVG will require only 2 treatments per year (Table 2). Hence, on the basis of efficacy and duration of action, IVG appears to be the more preferable choice among these injectable IVM formulations for the control of GI nematodes in a flock of sheep.

 

 

The outcome of the economic analysis shows that the average cost of a one-time treatment (Tc) for GI nematode infection using IVC, IVS and IVG for a group of 5 sheep are $20.6, $20.8 and $21.0, respectively. While the average annual costs of GI nematode control using IVC, IVS and IVG for a group of 5 sheep are $82.39, $83.22 and $41.99, respectively, as shown in Table 2.

A 20% increase or decrease in the average weight (AW) of the animals had the lowest impact on the average annual costs of GI nematode control (ATc) for all groups by increasing or decreasing the ATcby $0.004 for group A, $0.12 for B, and $0.1 for group C. The 20% increase or decrease in veterinary service cost (VSc) had the highest impact on the ATc for all the groups by increasing or decreasing the ATc by $4 for group A, $4 for group B and $2 for group C. Similarly, a 20% increase or decrease in veterinary visit costs (VVc); labour cost (Lc) and drug price (dp) increased or decreased the ATc as follows: $3.2 for group A, $3.2 for group B and $1.6 for group C; $2 for group A, $2 for group B and $1 for group C; $0.04 for group A, $0.12 for group B and $0.1 for group C respectively (Figures 2, 3 and 4).

 

 

 

 

 


 DISCUSSION

This study evaluated the  efficacy  of  three  different  IVM preparations in the treatment of GI nematodes in sheep as well as the onset of parasite re-infection after treatment. The efficacy of all three IVM preparations 7 days post treatment was 100% further strengthens claims about the susceptibility of GI nematodes to IVM in this region of Africa by Idika et al. (2012). Similarly, Peña-Espinoza et al. (2014)reported a 100% efficacy of IVM against H. contortus in small ruminants in Denmark. This finding is contrary to the report of anthelmintic resistance (AR) to all known anthelmintic groups including IVM in South Africa by Van Wyk et al. (1999). The difference may be due to a large scale sheep farming in South Africa and other southern hemisphere countries like Australia and New Zealand (Pomroy, 2006; Leathwick and Besier, 2014). These large-scale farms use IVM more frequently in GI nematode control as compared to the predominant small holder sheep farming structure in Nigeria. Periodic evaluation of the efficacy of common anthelmintic and possible resistance development by GI parasites is nevertheless important since AR has developed in sheep to all known anthelmintics except for monepantel (Kaminsky et al., 2011).

The different formulations of IVM (IVC, IVS and IVG) following clearance of infection prevented re-infection for a period of 28, 35 and 56 days, respectively. These differences in duration for re-infection to occur between treatment groups can be attributable to the different concentrations of IVM in the preparations used. The concentration of IVM in IVG may be responsible for the prolonged anthelmintic effect of IVG resulting from an extended  half-life  of the drug in plasma of treated sheep (McKellar and Marriner, 1987; Garg et al., 2007).

The economic model used to evaluate the comparative cost analysis of the three IVM preparations shows that in spite of the relatively large difference in price between the drugs (that is, $119.10 between the cheapest option, IVC and the most expensive option, IVG), the consequential difference in the average costs of a one-time treatment for a group of 5 sheep was relatively small, that is, $1.40 between the cheapest option (IVC) and the most expensive option (IVG). This may be due to the proportion of treatment  costs  attributable  to  the  cost  of  the  drug used was only about 0.5, 1.5 and 2.4% for IVC, IVS and IVG, respectively. Whereas, other complementary costs that make up the treatment costs contributed much more. The proportion of treatment costs attributable to veterinary service cost is almost 50% for all three treatment options. A scenario manipulation of the model showed that the cost of veterinary services would account for as much as 75% of treatment costs in a flock of 50 sheep kept under the same circumstances as those in the current study. The relatively high cost associated with veterinary services  make  farmers  to  by-pass  professionals  there by administering the drugs or employing the services of unqualified individuals (quacks). This abuse of the veterinary profession may increase the risk of anthelmintic resistance as a result of the use of incorrect dosages and routes of administration, as well as the practice of sub-optimal control strategies. Most farmers do not consider the cost of their labour (time and energy spent on catching and restraining the sheep during treatment) into account. This is taken for granted, but this study considered this an important input as persons may be employed to perform the duty. The farmer may perform the duty himself, the time spent should be valued based on the value  of  other  profitable  activities  he/she could have been engaged in during the period. In the current study, labour costs accounted for about 12% of treatment costs, which is much more than the cost of the drugs, indicating that they should not be overlooked. The sensitivity analysis buttresses the fact that veterinary services and labour costs are the highest contributors to the overall costs and should be considered more importantly in the choice of control strategy, rather than the price of the drug which is usually the major consideration by farmers.

The major reason for which IVG emerged as a cheaper option, this is less than half the cost of either IVC or IVS is  when   used  for  an  annual  control  programme.  The sheep were protected for 12 weeks, indicating that the treatment procedure will only need to be carried out twice a year as against four times when compared with the other two options used. This reduction in the frequency of treatment cuts down the cost of the procedure such as veterinary services and labour by 50%. This will reduce the exposure of the anthelmintic and possibly delaying the onset of anthelmintic resistance. Famers may be more willing to employ the services of a vet when the costs of veterinary services are lowered. To optimize the cost of anthelmintic control, the choice of anthelmintic should be based on the efficacy and duration of action of the drug.

 


 CONCLUSION

The GI nematode parasites in circulation among West African Dwarf (WAD) sheep in the study area may not have developed resistance to ivermectin. The IVG confers a longer duration of protection when compared with IVC and IVS formulations. While IVG is costly than both IVC and IVS in a one-time treatment of GI nematodes in sheep, it is much cheaper to use in an annual control programme of GI nematodes of sheep in the study area. Veterinary service and labour costs contributed more to treatment costs than the price of the anthelmintic in GI nematode control. Thus, the decision for choice of anthelmintic for optimization of the cost analysis of GI nematode control should be based on the efficacy and duration of action of the drug rather than its price.

 


 CONFLICT OF INTERESTS

The authors have not declared any conflict of interests.



 REFERENCES

Adamu M, Naidoo V, Eloff JN (2013). Efficacy and toxicity of thirteen plant leaf acetone extracts used in ethnoveterinary medicine in South Africa on egg hatching and larval development of Haemonchus contortus. BMC Veterinary Research 9(1):38. 
Crossref

 

Blackie S (2014). A Review of the epidemiology of gastrointestinal nematode infections in sheep and goats in Ghana. Journal of Agricultural Science 6(4):109-118. 
Crossref

 

Campbell WC (2012). History of avermectin and ivermectin, with notes on the history of other macrocycliclactone antiparasitic agents.CurrentPharmaceuticalBiotechnology13:853–865. 
Crossref

 

Campbell WC, Burg RW, Fisher MH, Dybas RA (1984). The discovery of ivermectin and other avermectins. Pesticide Synthesis through Rational Approaches pp. 5-20. 
Crossref

 

Campbell WC, Fisher MH, Stapley EO, Albers-Schönberg G, Jacob TA (1983). Ivermectin: a potent new antiparasitic agent. Science 221(4613):823-828. 
Crossref

 

Garg R, Kumar RR, Yadav CL, Banerjee PS (2007). Duration of anthelmintic effect of three formulations of ivermectin (Oral, Injectable and Pour-on) against multiple anthelmintic-resistant Haemonchus contortus in sheep. VeterinaryResearchCommunications 31(6):749-755. 
Crossref

 

Hansen J, Perry B (1990). The epidemiology, diagnosis and control of gastro-intestinal parasites of ruminants in Africa.International Laboratory for Research on Animal Diseases Nairobi.

 

Idika IK, Okonkwo EA, Onah DN, Ezeh IO, N Iheagwam C, Nwosu CO (2012). Efficacy of levamisole and ivermectin in the control of bovine parasitic gastroenteritis in the sub-humid savanna zone of southeastern Nigeria. Parasitology Research 111(4):1683-1687. 
Crossref

 

Jackson F, Coop RL (2000). The development of anthelmintic resistance in sheep nematodes. Parasitology 120(1984):S95–S107. 
Crossref

 

Kaminsky R, Bapst B, Stein PA, Strehlau GA, Allan BA, Hosking BC, Sager H (2011). Differences in efficacy of monepantel, derquantel and abamectin against multi-resistant nematodes of sheep. Parasitology Research 109(1):19-23. 
Crossref

 

Kenyon F, McBean D, Greer AW, Burgess CGS, Morrison AA, Bartley DJ, Jackson F (2013). A comparative study of the effects of four treatment regimes on ivermectin efficacy, body weight and pasture contamination in lambs naturally infected with gastrointestinal nematodes in Scotland. InternationalJournal forParasitology:Drugs Drug Resistance 3:77-84. 
Crossref

 

Kumar N, Rao TKS, Varghese A, Rathor VS (2013). Internal parasite management in grazing livestock. Journal of Parasitic Diseases
Crossref

 

Leathwick DM, Besier RB (2014). The management of anthelmintic resistance in grazing ruminants in Australasia - Strategies and experiences. Veterinary Parasitology 204(1):44-54. 
Crossref

 

McKellar Q, Marriner S (1987). Comparison of the anthelmintic efficacy of oxfendazole or ivermectin administered orally and ivermectin administered subcutaneously to sheep during the periparturient period. Veterinary Record 120(16):383-386. 
Crossref

 

Melaku A, Bogale B, Chanie M, Fentahun T, Berhanu A (2013). Study on utilization and efficacy of commonly used anthelmintics against gastrointestinal nematodes in naturally infected sheep in North Gondar, North-Western Ethiopia. African Journal of Pharmacy and Pharmacology 7(12):679–684.
Crossref

 

Merola VM, Eubig PA (2012). Toxicology of avermectins and milbemycins (macrocylic lactones) and the role of P-glycoprotein in dogs and cats. Veterinary Clinics of North America: Small Animal Practice 
Crossref

 

Molento MB (2009). Parasite control in the age of drug resistance and changing agricultural practices. Veterinary Parasitology 163(3):229-234. 
Crossref

 

Nolan T (2012). Macrocyclic lactones in the treatment and control of parasitism in small companion animals. Current Pharmaceutical Biotechnology 13:1078-1094. 
Crossref

 

Nwosu CO, Madu PP, Richards WS (2007). Prevalence and seasonal changes in the population of gastrointestinal nematodes of small ruminants in the semi-arid zone of north-eastern Nigeria. Veterinary Parasitology 144(1):118-124.
Crossref

 

Pe-a-Espinoza M, Thamsborg SM, Demeler J, Enemark HL (2014). Field efficacy of four anthelmintics and confirmation of drug-resistant nematodes by controlled efficacy test and pyrosequencing on a sheep and goat farm in Denmark. Veterinary Parasitology 206(3-4):208-215. 
Crossref

 

Pomroy WE (2006). Anthelmintic resistance in New Zealand: a perspective on recent findings and options for the future.The New Zealand Veterinary Journal 54(6):265-270. 
Crossref

 

Roeber F, Jex AR, Gasser RB (2013). Impact of gastrointestinal parasitic nematodes of sheep, and the role of advanced molecular tools for exploring epidemiology and drug resistance - an Australian perspective. Parasites and Vectors 6:1. 
Crossref

 

Shoop WL, Mrozik H, Fisher MH (1995). Structure and activity of avermectins and milbemycins in animal health. Veterinary Parasitology 59(2):139-156. 
Crossref

 

Singh R, Ba MS, Singla LD, Kaur P (2017a). Detection of anthelmintic resistance in sheep and goat against fenbendazole by faecal egg count reduction test. Journal of Parasitic Diseases 41 (2):463-466.
Crossref

 

Singh E, Kaur P, Singla LD, Bal MS (2017). Prevalence of gastrointestinal parasitism in small ruminants in western zone of Punjab, India. Veterinary World 10(1):61-66.
Crossref

 

Singh V, Varshney P, Dash SK, Lal HP (2013). Prevalence of gastrointestinal parasites in sheep and goats in and around Mathura, India. Veterinary World 6(5):260-262. 

 

Singla LD (1995) A note on sub-clinical gastro-intestinal parasitism in sheep and goats in Ludhiana and Faridkot districts of Punjab. Indian Veterinary Medical Journal 19:61-62.

 

Van Wyk JA, Stenson MO, Van der Merwe JS, Vorster RJ, Viljoen PG (1999). Anthelmintic resistance in South Africa: surveys indicate an extremely serious situation in sheep and goat farming. Onderstepoort Journal of Veterinary Research 66(4):273-284.

 

Waller PJ (1997). Sustainable helminth control of ruminants in developing countries. Veterinary Parasitology 71:195-207. 
Crossref

 

Waller PJ (2006). Sustainable nematode parasite control strategies for ruminant livestock by grazing management and biological control. Animal Feed Science and Technology 
Crossref

 

Zinsstag J, Ankers P, Ndao M, Bonfoh B, Pfister K (1998). Multiparasitism, production and economics in domestic animals in sub-Saharan West Africa. Parasitology Today 14(2):46-49. 
Crossref

 

Zvinorova PI, Halimani TE, Muchadeyi FC, Matika O, Riggio V, Dzama K (2016). Prevalence and risk factors of gastrointestinal parasitic infections in goats in low-input low-output farming systems in Zimbabwe. Small Ruminant Research 143:75-83. 
Crossref

 




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