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Friday, 31 May 2019

Is There Any Evidence to Support the Use of Garlic as a Wormer for Dogs and Cats in the UK?

a Knowledge Summary by
Louise Buckley PhD, RVN 1*
1The Royal (Dick) School of Veterinary Studies, University of Edinburgh
*Corresponding Author (louise.buckley@ed.ac.uk)
Vol 4, Issue 2 (2019)
Published: 29 May 2019
Reviewed by: Virginia Fajt (DVM, PhD, DACVCP) and William Chandler (BVetMed, MRCVS)
Next review date: 20 Feb 2021
PICO question
In dogs and cats, is the oral administration of garlic, compared to no treatment, efficacious at preventing or reducing the intestinal worm burden (species found in the UK)?
Clinical bottom line
No studies were identified that investigated the efficacy of garlic at preventing intestinal worm burden. Garlic reduced egg and/or larvae counts in the worm species studied. However, where measured, egg and larvae count rapidly (2 days) returned to pretreatment levels once dietary garlic was discontinued. None of the studies included adulticidal action as an outcome measure. In the absence of research to demonstrate high levels of adulticidal action against a range of intestinal wormers at therapeutic, non-toxic levels in cats and dogs, clients should be advised that garlic has not been demonstrated to be an effective anthelmintic (either for multiple or single species use) for use in dogs and cats either to prevent or to treat an intestinal worm burden.
Clinical scenario
The veterinary nurse is reading through the worming advice being given in a Facebook group that encourages a natural approach to preventative medicine in dogs and cats. She notices that garlic is being recommended quite frequently by some pet owners as an alternative to a conventional anthelmintic and wonders what the evidence base is for this recommendation. She notes that some owners are recommending its routine use to prevent dogs or cats becoming parasitised and others are recommending it for dogs or cats known to have an intestinal worm burden so she includes both aspects in her PICO.
The evidence
No papers were identified that addressed the use of garlic to prevent dogs and/or cats becoming parasitised by intestinal worm species. Three papers were identified that either fully (Bastidas, 1969; Ronagh et al. 2015) or partially (Andrei et al., 2011) addressed the intestinal worm reduction aspect of the PICO. Two of the studies focused on dogs (Bastidas, 1969; Andrei et al., 2011) and one of the studies focused on cats (Ronagh et al., 2015). Not all species of intestinal worm known to parasitise cats and/or dogs in the UK were represented, with tapeworm species being the notable exception. All three studies were clinical trials that either used the animal as its own control (Andrei et al., 2011, Bastidas, 1969) or allocated the animals to separate treatment groups (Ronagh et al., 2015). Random allocation of the latter was not reported. Despite being clinical trials, all three studies are very limited with poor data handling and insufficient reporting of the methodology and/or results.
The Andrei et al. (2011) study used the garlic in conjunction with other herbs so any potential anthelmintic effect of garlic is totally confounded with the other components (n = 6, plus water) of the tincture and pumpkin oil preparation used. However, this tincture was associated with a greater than 90% reduction in eggs per gram of faeces for all species (Toxocara canis, Ancylostoma spp., Trichocephalus spp.), with similar findings across both populations (shelter dogs: n = 37, owned dogs: n = 10)) studied. Bastidas (1969), with a sample size of one, found that larvae count of Ancylostoma Caninum decreased during daily dosing with garlic, but eggs per gram of faeces was only slightly reduced. Rapid recovery to pre-dosing levels (2 days) was observed following treatment cessation. Finally, Ronagh et al. (2015) found that cats dosed with garlic (n = 5) showed a numerical reduction in Toxocara cati eggs on a faecal egg count and a numerical reduction in fecundity rate (number of eggs produced by a female adult Toxocara cati worm). No such reduction in either parameter was observed for Control cats (n = 5). None of the studies directly studied the effect of garlic as an adulticide and this remained an important practical limitation in the use of these findings.
Summary of the evidence
Andrei et al. (2011)
Bastidas (1969)
Ronagh et al. (2015)
Appraisal, application and reflection
Plant-based anthelmentics have been suggested as a potential alternative to overcome increasing resistance to conventional anthelmentics (French, 2018). The use of garlic as a traditional anthelmintic for dogs with intestinal worms has been reported (n = 1 interviewee) in a study exploring central-southern Italy’s ethno-veterinary practices (Guarrera et al., 2008), and more widely elsewhere in pigs (Lans et al., 2007; Bartha et al., 2015) and ruminants (Lans et al., 2007; Bullitta et al., 2018). Thus, the promotion of garlic as an anthelmintic in dogs and cats is probably derived from traditional ethnobotanical medical practices. More recently, there has been some growth in scientific interest in its potential anthelmintic properties in a range of mammalian and avian species. Extracts from garlic bulbs shown to have in vivo (e.g. Palacious-Landin et al., 2015, but see e.g. Worku, 2009; Velkers et al., 2011) and/or in vitro (e.g. Palacious-Landin et al., 2015; Orengo et al., 2016; Tavassoli et al., 2018) efficacy (differing stages of the life cycle, dependent on the study) against various species of helminth. This includes in vitro activity against some species (Toxocara canis, Ancylostoma caninum) that infest dogs (Orengo et al., 2016). Consequently, scientific and veterinary growth in its interest in a wormer for dogs and cats may be likely to develop over time.
No English language papers were identified that addressed the prevention aspect of the PICO. Three papers were identified that either fully (Bastidas, 1969; Ronagh et al., 2015) or partially (Andrei et al., 2011) addressed the treatment aspect of the PICO. Two of the studies focused on dogs (Bastidas, 1969; Andrei et al., 2011) and one of the studies focused on cats (Ronagh et al., 2015).  A further abstract (Bekirov et al., 1979) that examined the use of garlic (in conjunction with other ingredients) as a canine anthelmintic effective against Echinococcus or Taenia hydatigena was excluded as the main paper was in Russian but reported 92–94.8% and 100% efficacy respectively against each species. The relative lack of studies that addressed the PICO also meant that some of the intestinal worms known to affect dogs and cats in the UK did not have any evidence available to address the use of garlic as an anthelmintic for that species. Studies focusing on tapeworm species were notably absent, with the exception of the Bekirov study, which combined garlic with several other products thereby confounding interpretation of the efficacy of garlic per se as an anthelmintic. Thus, any positive anthelmintic effects at the level of the individual species may still limit clinical use to the practitioner or owner when seeking an anthelmintic effective against a broad range of intestinal worms.
All three studies included in this Knowledge Summary were clinical trials, which either used the animal as its own control (Andrei et al., 2011, Bastidas, 1969) or allocated the animals to separate treatment groups (Ronagh et al., 2015). However, despite being clinical trials, all of the studies showed clear limitations in terms of methodological approach and/or study methodology reporting and/or results reporting and highlight the importance of not using the evidence pyramid (see: O’Connor, 2017 for a discussion on the limitations to the evidence pyramid) in isolation when evaluating the relative quality of a study. Furthermore, the outcome measures used by each of the studies used are unlikely to address the clinical need of veterinary practitioners or clients seeking an anthelmintic that will kill intestinal worms present at the point of dosing the dog or cat.
In the Andrei et al. (2011) study a 90% reduction in eggs per gram of faeces for all species (Toxocara canis, Ancylostoma spp, Trichocephalus spp.) following a twice daily weight dependent dose of their worming preparation (tincture and pumpkin oil). Similar results were obtained for both populations (shelter dogs: n = 37, owned dogs: n = 10)) studied. However, this worming preparation used the garlic in conjunction with other herbs so any potential anthelmintic effect of garlic is totally confounded with the other components (n = 6, plus water) of the tincture and pumpkin oil preparation used. Thus, it is impossible to quantify the relative contribution (positive, negative, additive, synergistic, or no effect at all) of garlic to these findings. In defence of the authors, this study was designed to test the efficacy of this worming preparation rather than to investigate the efficacy of garlic in isolation as an anthelmintic. However, this study is also problematic in terms of its scientific quality, with authors failing to report tincture composition in sufficient detail, with no detail available on the quantity of each herb added to the tincture preparation. Dosing standardisation was achieved through product dosing based on the weight of the dog, but this is only described in terms of quantity of the tincture plus pumpkin oil supplied. Despite the most impressive sample size (relative to the other two studies reported here), the authors do not perform analytical statistics on their findings, and while they describe reporting the confidence intervals (which can be used in preference to p values), they appear to be reporting this as one value rather than as an upper and lower limit which limits its value in interpreting the data. However, the descriptive statistics do suggest that the before and after treatment faecal egg counts would be significantly different across all three of the worm species studied (and the direction of the effect is similar for both shelter and owned dogs) should a suitable analytical test be performed. Despite this, the study suffers from another key issue when considering the clinical application of this tincture, and that is that the outcome measure assessed did not include either a direct or indirect (proxy) measurement of the effect of the preparation on adult worm mortality and/or long-term fecundity. The study finished immediately after the end of the tincture and pumpkin oil dosing period. Thus, all that is known is that this worming preparation had effects on egg production during the period of dosing, without anything to indicate the possible reason for this reduction. This is a clinically important issue that is of relevance to any anthelmintic product selection, and represents a major study limitation within the context of any clinician considering using this worming preparation in preference to any product with known adulticidal efficacy.
The second of the studies evaluated (Bastidas, 1969) was included as a clinical trial based on its study methodology (before, during, after treatment) allowing it to meet the inclusion criteria but it had a sample size of one dog, and with each study phase undertaken only once, findings were potentially explicable, either partially or fully, by other undefined or unreported effects. This should be borne in mind when considering the reported findings. This study found that larvae count of Ancylostoma caninum decreased during daily dosing with garlic (non-standardised dose), but eggs per gram of faeces remained similar following a five-day dosing period. Application of the Andrei et al. (2011) equation for evaluating anthelmintic efficacy to Bastidas’ (1969) raw data indicated that efficacy at reducing egg count after 5 days of garlic treatment was only 14.75%. This was much lower than the Andrei et al. (2011) study, and suggests that other components of the Andrei et al. study’s worming preparation may have explained the increased efficacy at reducing egg count identified in that study. However, there are other differences in the study methodology and lack of detail regarding the tincture preparation mean that meaningful comparisons are difficult to draw. Garlic appeared more effective at reducing larvae count and was 81.77% effective at reducing larvae count by day 5 (the last day) of treatment. However, it is important to note that this effect was very short lived and mean larvae count increased rapidly (1 day) following discontinuation of the garlic and returned to approximately pretreatment levels only 2 days after discontinuation of the garlic. Again, while the presence of viable adult female worms was not an outcome measure of this study, these post-treatment changes in larvae count suggest that the addition of garlic to the diet at this dosage and dosing period did not affect adult female worm mortality or longer-term fecundity rates.
Finally, Ronagh et al. (2015) found that cats dosed with garlic (n = 5) showed a numerical reduction in Toxocara cati eggs on a faecal egg count and a numerical reduction in fecundity rate (number of eggs produced by a female adult Toxocara cati worm). No such reduction in either parameter was observed for Control cats (n = 5). However, this study euthanised the cats at the end of the study (to assess fecundity rate and gastrointestinal damage to the mucosa) and did not measure faecal egg counts for a few days post-treatment cessation. Thus, while it is known that egg counts were lower, and this reduction was probably due to a reduction in the number of eggs produced by each viable female, it is not known whether any inhibitory effect of the garlic is temporary (i.e. females will increase egg production when the garlic is discontinued) or whether it is more permanent (e.g. through increased morbidity/mortality rates of adult female worms). In the light of the Bastidas (1969) study findings this is an important consideration. This study did count the number of adult female worms present within the intestines at the point of euthanasia of both the Control group and the Garlic group but does not report this information. However, the authors do not report how the cats were allocated to their respective treatment groups. Frustratingly, the pretreatment faecal egg count demonstrates that the Control cats had a lower mean (± standard deviation) faecal egg count (9.4 ± 1.1) and fecundity rate (6.4 ± 2.0) than the Garlic group (egg count: 19.0 ± 2.0; fecundity rate: 10.4 ± 3.5), with important implications for data handling, analysis and interpretation. The authors’ report a significant effect of treatment group (Garlic versus Control) but fail to report what data was analysed to obtain this probability value, and its value to the data interpretation is thereby questionable. With better management of subject allocation to the treatment groups (for example by using faecal egg counts to rank cats according to worm burden severity and then allocating to treatments using a randomised block approach) this study could have been strengthened. It is not clear why this was not undertaken as the authors originally trapped 100 cats, and retained the 25 most Toxocara cati parasitised cats to use in this study, so this limitation could have been addressed at the study outset.
In summary, based on the limited and relatively poor quality studies available to address the PICO, garlic may have a temporary inhibitory action on larvae and/or egg production of the intestinal worm species studied but none of the studies directly investigated the effect of garlic on adult worm mortality or viability. However, where a proxy measure was used (egg/larvae production after treatment cessation) this suggested that garlic did not have adulticidal action against Ancyclostoma caninum. In the absence of research to demonstrate high levels of adulticidal action against a range of intestinal wormers at therapeutic, non-toxic levels in cats and dogs, clients should be advised that garlic is not proven as an effective anthelmintic (either against multiple species or a single species) for use in dogs and cats with to prevent, or to treat, an intestinal worm burden.
Methodology Section
Search Strategy
Databases searched and dates covered:Pubmed, accessed  via the NCBI website (01/01/1900 – 20/02/2019); Web of Science (1990 – 20/02/2019)
Search terms:Pubmed & Web of Science search:
(dog OR dogs OR canine OR canid OR canis OR bitch OR bitches OR pup OR puppy OR puppies OR cat OR cats OR feline OR felid OR kitten OR kittens) AND (garlic OR “allium sativum”) AND (worm OR tapeworm OR tape-worm OR “tape worm” OR roundworm OR round-worm OR “round worm” OR hookworm OR hook-worm OR “hook worm” OR whipworm OR whip-worm OR “whip worm” OR flatworm OR “flat worm” OR flat-worm OR endoparasite OR endo-parasite OR parasite OR parasitic OR anthelmintic OR ascarid OR ascaris OR larvae OR toxocara OR toxascaris OR ancylostoma OR trichuris OR uncinaria OR Dipylidium OR Taenia OR echinococcus OR cestode OR cestodes OR nematode OR nematodes OR Trematode OR Trematodes OR Fluke OR Flukes OR Nanophytus OR heterophyes OR cryptocotyle OR apophallus OR alaria)
CAB Abstract search:
  1. (dog or dogs or canine or canid or canis or bitch or bitches or pup or puppy or puppies or cat or cats or feline or felid or kitten or kittens).mp. [mp=abstract, title, original title, broad terms, heading words, identifiers, cabicodes]
  2. (garlic or allium sativum).mp. [mp=abstract, title, original title, broad terms, heading words, identifiers, cabicodes]
  3. (worm or tapeworm or tape-worm or tape worm or roundworm or round-worm or round worm or hookworm or hook-worm or hook worm or whipworm or whip-worm or whip worm or flatworm or flat worm or flat-worm or endoparasite or endo-parasite or parasite or parasitic or anthelmintic or ascarid or ascaris or larvae or toxocara or toxascaris or ancylostoma or trichuris or uncinaria or Dipylidium or Taenia or echinococcus or cestode or cestodes or nematode or nematodes or Trematode or Trematodes or Fluke or Flukes or Nanophytus or heterophyes or cryptocotyle or apophallus or alaria).mp. [mp=abstract, title, original title, broad terms, heading words, identifiers, cabicodes]
  4. 1 and 2 and 3
Dates searches performed:Pubmed (20/02/2019); Web of Science (20/02/2019); CAB Abstracts (20/02/2019)
Exclusion / Inclusion Criteria
Exclusion:Pre-defined exclusion criteria: non-English language, popular press articles, in vitro studies, conference abstracts
Inclusion:Any comparative study in which the effect of garlic on intestinal worms in dogs or cats was studied
Search Outcome
Database
Number of results
Excluded – did not answer the PICO question
Excluded – not English language
Excluded – conference abstract only
Excluded – duplicates
Total relevant papers
Pubmed
870001
Web of Science
1000000
CAB Abstracts
17141002
Total relevant papers when duplicates removed
3
Conflict of Interest
The author declares no conflicts of interest.
References
  1. Andrei, S., Ilie, M. S., Mederle, N. & Darabus, G. (2011) Testing the effectiveness of a plant extract in the therapy on some endoparasites in dogs. Lucrari Stiintifice - Medicina Veterinara, Universitatea de Stiinte Agricole si Medicina Veterinara "Ion Ionescu de la Brad" Iasi, 54(3), pp. 247–254.
  2. Bartha, S. G., Quave, C. L., Balogh, L., Papp, N. (2015) Ethnoveterinary practices of Covasna County, Transylvania, Romania. Journal of Ethnobiology and Ethnomedicine 11: 35 [online] Available from: https://ethnobiomed.biomedcentral.com/articles/10.1186/s13002-015-0020-8 (accessed: 16/05/2019) DOI: http://dx.doi.org/10.1186/s13002-015-0020-8
  3. Bastidas, G. J. (1969) Effect of ingested garlic on Necator americanus and Ancylostoma caninum. The American Journal of Tropical Medicine and Hygiene, 18(6), pp. 920–923. DOI: http://dx.doi.org/10.4269/ajtmh.1969.18.920
  4. Bekirov, R. E., Azimov, Sh. A., Oripov, A. O., & Dzhumaev, Z. (1979) The efficacy of granules against cestodes in dogs. Veterinariya, Moscow 8, pp. 50–51.
  5. Bullitta, S., Re, G. A., Manunta, D. I., & Oiluzza, G. (2018) Traditional knowledge about plant, animal, and mineral-based remedies to treat cattle, pigs, horses, and other domestic animals in the Mediterranean island of Sardinia. Journal of Ethnobiology and Ethnomedicine 14: 50 [online] Available from: https://ethnobiomed.biomedcentral.com/articles/10.1186/s13002-018-0250-7 (accessed: 16/05/2019) DOI: http://dx.doi.org/10.1186/s13002-018-0250-7
  6. Buona, F., Pacifico, L., Piantedosi, D., Sgroi, G., Neola, B., Roncoroni, C., Genovese, A., Rufrano, D., & Veneziano, V. (2019) Preliminary Observations of the Effect of Garlic on Egg Shedding in Horses Naturally Infected by Intestinal Strongyles. Journal of Equine Veterinary Science 72: 79–83. DOI: http://dx.doi.org/10.1016/j.jevs.2018.10.025
  7. French, K. E. (2018) Plant-Based Solutions to Global Livestock Anthelmintic Resistance. Ethonobiology Letters 9(2): 110–123. DOI: http://dx.doi.org/10.14237/ebl.9.2.2018.980
  8. Guarrera, P. M., Lucchese, F., & Medori, S. (2008) Ethnophytotherapeutical research in the high Molise region (Central-Southern Italy). Journal of Ethnobiology and Ethnomedicine 4: 7 [online] Available from: https://ethnobiomed.biomedcentral.com/articles/10.1186/1746-4269-4-7 (accessed: 16/05/2019) DOI: http://dx.doi.org/10.1186/1746-4269-4-7
  9. Lans, C., Turner, N., Khan, T., Brauer, G., & Boepple, W. (2007) Ethnoveterinary medicines used for ruminants in British Columbia, Canada. Journal of Ethnobiology and Ethnomedicine 3: 11 [online] Available from: https://ethnobiomed.biomedcentral.com/articles/10.1186/1746-4269-3-11 (accessed: 16/05/2019) DOI: http://dx.doi.org/10.1186/1746-4269-3-11
  10. O’Connor, A. (2017) Is the simplicity of the evidence pyramid actually detrimental for understanding evidence? Veterinary Evidence 2(1).  DOI: http://dx.doi.org/10.18849/ve.v2i1.100
  11. Orengo, K. O., Maitho, T., & Mbaria, J. 2016. In vitro anthelmintic activity of Allium sativum, Allium cepa and Jatropha curcas against Toxocara canis and Ancylostoma caninum. African Journal of Pharmacy and Pharmacology 10(21): 465–471.
  12. Martin, L. K. & Beaver, P. C. (1968) Evaluation of Kato thick-smear technique for quantitative diagnosis of helminth infections. American Journal of Tropical Medicine and Hygiene 17, pp. 382–391. DOI: http://dx.doi.org/10.4269/ajtmh.1968.17.382
  13. Palacious-Landin, J., Mendoza-de Gives, P., Salinas-Sanchez, D. O., Lopez-Arellano, M. E., Liebano-Hernadez, E., Hernadez-Velazquez, V. M., & Valladares-Cisneros, M. G. (2015) In vitro and in vivo nematocidal activity of Allium sativum and Tagetes erecta extracts Against Haemonchus contortus. Turkish Journal of Parasitology 31: 277–282. DOI: http://dx.doi.org/10.5152/tpd.2015.4523
  14. Ronagh, K., Gharouni, A., Bahadori, S. R., Zakian, A., Gholami, N., Rezaeian, H. & Shahraki, M. S. (2015) Effect of Nigella sativa, Allium sativum, Syzgium aromaticum and Cucurbita maxima on Toxocara cati fecal egg count in stray cats. Online Journal of Veterinary Research, 19(5), pp. 325–330.
  15. Tavassoli, M., Jalilzadeh-Amin, G,. Fard, V. R. B., & Esfandiarpour, R. 2018. The in vitro effect of Ferula asafoetida and Allium sativum extracts on Strongylus spp. Annals of Parasitology 64(1): 59–63.
  16. Velkers, F. C., Dieho, K., Pecher, F. W. M., Vernooij, J. C. M., van Eck, J. H. H., &Landman, W. J. M. (2011) Efficacy of allicin from garlic against Ascaridia galli infection in chickens. Poultry Science 90(2): 364–368. DOI: http://dx.doi.org/10.3382/ps.2010-01090
  17. Worku, M., Franco, R., & Baldwin, K. (2009) Efficacy of garlic as an anthelmintic in adult Boer goats. Archives of Biological Sciences 61(1): 135–140. DOI: http://dx.doi.org/10.2298/ABS0901135W

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