Veterinary Parasitology 84 (1999) 337–347

Important parasites in poultry production systems
Michael D. Ruff ∗
Beltsville Agricultural Research Center, Agricultural Research Service, United States Department of Agriculture, Beltsville, MD 20705, USA

Abstract Poultry now accounts for 30% of all meat consumed. Parasites are a problem where ever poultry are raised, whether in large commercial operations or in small back-yard flocks, and economic losses can be significant. This paper will briefly review the major protozoan, helminth, and arthropod species in poultry including pathogenesis. Other topics will include the importance of the interaction of other diseases and parasites, and control of the infection by chemotherapy, management, and immunity. Published by Elsevier Science B.V.
Keywords: Parasites; Poultry

1. Introduction The demand for poultry meat is increasing throughout the world. Per capita consumption increased from 23 kg in 1975 to 28 kg in 1995 and is projected to reach 31 kg by 2000 and now accounts for 30% of all meat consumed according to the FAO. Increased production will require an additional 100 million tons of feed. The largest producer, the US, has increased its broiler exports 450% since 1990. Parasites are a problem where ever poultry are raised and can have adverse economic effects on production parameters. The method of rearing has a marked effect on the particular problem that is seen. Confinement rearing tends to favor those parasites with short life cycles and direct transmission such as Eimeria spp., Ascaridia galli, Heterakis gallinarum, and Capillaria spp. The rearing of free-range birds or back yard flocks provides an opportunity for parasites that require an intermediate host. It should be remembered that parasitism in poultry is a flock problem; what happens to an individual bird is of relatively little economic importance. It is not the purpose of this paper to give a check list of poultry parasites or to describe them or their life cycles in detail.

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losses from decreased weight gain and feed efficiency and the cost of treatment are estimated by Weber (1997) to annually exceed US$ 1. Chilomastixand Hexamita. but from the standpoint of the poultry producer. McDougald and Reid. For example. any of them can cause a problem if present in large enough numbers. 1997).5 billion world wide.01 kg less feed required per kg of gain) would save the US poultry industry over US$ 70 million based on current production numbers (Ruff and Danforth. Ruff / Veterinary Parasitology 84 (1999) 337–347 Rather it will touch briefly on the more economically important ones with comments on control measures and why problems still exist. . Trypanosoma. Japanese quail. Haemoproteus. Leucocytozoon. The role of the cecal worm. but all species of avian Eimeria produce weight loss.1. and decreased egg production. increased feed conversion ratios. and even new farms will have the parasite present within a few weeks after poultry are introduced (Ruff and Wilkins. chickens.338 M. both in terms of distribution. 1997). 2. large or small. Heterakis gallinarum. an increase in feed efficiency of 1/100 of a point (0. turkeys. unpublished data. especially in turkeys. frequency.D. Mortality. Flagellates such as Histomonas. 1996). 1993). and amoeba of the genera Entamoeba and Endolimax are also found. and economic losses (McDougald and Reid. Transmission from one farm to another is facilitated by movement of personnel and equipment. loss of skin pigment. Coccidiosis Coccidia are without question the most important parasites of poultry. Some species tend to be more pathogenic in terms of the inoculation dose required to produce measurable effects. have coccidia present is the extreme reproductive ability of these intracellular parasites. To give an idea of how little effect it takes to have an economic impact. and a microsporidian. Encephalitozoon cunicule has recently been reported from chickens (Reetz. Protozoa The most important protozoa infecting poultry belong to the phylum Apicomplexa which includes genera the Eimeria. primarily in turkeys but occasionally in chickens and game birds. only Histomonas meleagridis infections sometimes reach a level of major economic importance. and earthworms in transmission and the necessity for certain bacterial flora to cause pathogenicity are well documented (McDougald. Although mortality from coccidiosis is under control by anticoccidial medications. pheasants. Sarcocystis and Cryptosporidium. Other protozoa of the digestive tract Of the other protozoa that infect the digestive tract.2. Each oocyst ingested by the host may give rise to hundreds of thousands infective oocysts in the feces within 7–12 days. Avian coccidia of the genus Eimeria are extremely host specific. Differences in species within a host are of academic and physiological interest. 2. and bobwhite quail all have their own species. Trichomonas. One reason that all poultry production units. 1997). 2. 1979. Toxoplasma.

Plasmodium gallinaceum.D. both in terms of number of species and pathology. Levy. durae are the most pathogenic for domestic fowl and may cause mortality of over 90% (Kemp.3.M. The latter species was responsible for the failure of a large commercial turkey production effort in the coastal plains and sandhill areas of South Carolina (Dick.. Ruff / Veterinary Parasitology 84 (1999) 337–347 339 chukar partridge. 1984). simondi (ducks and geese). P. 1986. Effective medications for these infections are limited or lacking so prevention of infection is the best means of control. Infection rates in some areas can be as high as 100% (Springer.. caulleryi (chickens). and ruffed grouse can be quite high. as well as Capillaria spp. Ascaridia. Capillariaand Syngamus (gapeworm) are generally the most common nematodes encountered in commercial poultry operations. There other genera such as Dispharynx. 1971a. For a detailed listing the reader is referred to Ruff and Norton (1997) for poultry and game birds. Over 65 species of Plasmodium have been described from different birds. baileyi. 1987). Avian plasmodia develop in mosquitoes of the genera Culex and Aedes. Subulura and Trichostrongylus are found far more frequently than in confinement facilities. Gongylonema. Various dipteran intermediate hosts. smithi (turkeys) although other species are also described (Springer. especially those species that utilize an intermediate host (Permin et al. 1955). 1988. 1978). and McDonald (1969) for waterfowl. Another species. . b). are responsible for the transmission so infections can arise in those areas where they are present. 1984. Hoerr et al. Blood and tissue protozoa Leucocytozoon infects the blood and tissue cells of internal organs. 1997). galli is the finding of this parasite inside of the hen’s egg (Reid and McDougald. Sarcosporidiosis can be a major problem in waterfowl and many species of birds can be infected with Toxoplasma. A third. An occasional aesthetic problem with A. Current. currently unnamed.. The three main species are L. but are not generally a problem in broiler chickens because of the short grow out time. Infection of turkeys with C. Current et al. personal communication. Tetrameres. Heterakis. and rarely in Anopheles. 1986). Species of the genera Ascaridia. Over 120 species of Haemoproteus have been reported from birds but they seem to cause few problems. 3. 1997). sometimes with high prevalence rates. Nematodes Nematodes constitute the most important group of poultry helminths. species can cause up to 100% mortality in bobwhite quail (M. L. juxtanucleare and P. infects both the digestive tract and respiratory tract of chickens and turkeys (Current et al. 1997).. but Kemp (1978) considers less than 35 valid. Cryptosporidium can cause severe problems in some species of poultry (Lindsay et al.. 1978). Capillaria and Syngamus can produce significant growth depression and mortality in pen raised game birds. such as simuliid flies and culicoid midges. can cause production losses in breeders. and L. meleagridis can cause diarrhea and mild mortality (Slavin. Ascarids can reduce weight gain and feed efficiency (Ikeme. 2. 1997). to Kellog and Calpin (1971) for quail. Nematodes can be a more serious problem in backyard flocks in developing countries. C..

Nadakal and Nair. but has lessened the frequency of lice problems (fewer ages of birds on the same farm) and chicken mites (fewer hiding places). Often the acanthocephalans are larval forms suggesting that the infections are accidental. 6. Over 500 species of trematodes have been reported from birds. sticktight fleas) than for those that are on the bird only to feed (bedbugs. Exceptions are the microscopic tapeworm Davainea proglottina and Raillietina tetragona where decreases in weight gain and egg production have been documented following experimental infections (Levine. Ruff / Veterinary Parasitology 84 (1999) 337–347 4. Ectoparasites There are several types of arthropods that constitute the major ectoparasites of poultry. Insects Only chewing lice of the order Mallophaga infect birds. modern high-density production units have favored the northern fowl mite. Cestodes Cestodes (tapeworms) are commonly encountered in poultry from free-range or backyard flocks. especially in poultry from back yard flocks or pet birds. 1979). Other helminths Acanthocephalans (spiny headed worms) and trematodes (flukes) are infrequently found in poultry. a study in the arid zone of Nigeria found an infection rate of 56% for cestodes. 1993). soft ticks). especially with infections of only a few hundred worms. Conversely. In US. especially in broilers.. 1997). The economic . the reader is referred to Reid and McDougald (1997). mites and ticks. 1938. This fluke utilizes two intermediate hosts (snail and dragon fly). Pathology is usually mild. the oviduct fluke. 1994).1. Host specificity is fairly broad for most species so the diagnostition may encounter adults or larval metacercaria in almost any cavity or tissue. 5. 6. fleas. The degree and type of infestation is markedly influenced by the production method. For brief descriptions of individual species. Detection is important and easier for those parasites that live on the bird (lice. chicken mites. northern fowl mites. primarily lice. compared with a 16% infection rate for nematodes (Ahmed and Sinha. these systems have favored infestation with Dermanyssus gallinae. More than 40 species have been reported from domestic birds. and host specificity is relatively low. yet a recent 1-year study in Arkansas found Raillietina cesticillus in almost 70% of the broiler farms examined (Wilson et al. in countries such as Denmark.. Most species of cestodes seem to cause little pathology of economic importance. Most poultry producers in US will state that cestodes are only an infrequent problem in commercial operations. some 20 are considered to be potentially dangerous to poultry (Kingston. bugs. Some species and locations are described by Kingston (1984) and Reid and McDougald (1997). hard ticks. Similarly.D.340 M. One of the more frequently found is Prostogonimus spp. 1984). 1997). Ornithonyssus sylviarum in layer and breeder houses (Arends. The adult develops in the oviduct and drastically reduces egg production (Reid and McDougald.

Although many Diptera will feed on poultry (mosquitoes. and in the respiratory system. In heavy infestations. is especially harmful to nestling pigeons and also transmits Haemoproteus columbae which causes a malarial-like disease of pigeons. the feathers may be blackened. Other mites are found on or in the quills. Black flies. causing prominent abbesses that result in down grading at processing because the skin lesions must be trimmed (Loomis. larvae attach to the skin. found no effect on laying hens. Pseudolynchia canariensis. Several genera of mosquitoes can transmit avian Plasmodium spp. piroplasmosis. In many tropical countries it has prevented the rearing of imported breeds (Reid. midges. Echidnophaga gallinacea.. Cimex lectularius. Blood loss from the feeding of larvae and nymphs of soft ticks may even cause fatal anemia. are important for the transmission of Leucocytozoon spp. Death can result in young and adult birds. 1997). 1984). is rare in caged-layer operations in US. Another problem is that mites often leave the bird when infestations are heavy and attack poultry workers or infest nearby dwellings (Arends. In warmer regions of the world the tropical fowl mite replaces the norther fowl mite with the same severe pathology. and bacterial diseases of importance in many parts of the world.M. The adults are usually attached to the skin of the head of the host in clusters of up to 100. Regardless. gnats. Some authors (Warren et al. to poultry such as turkeys and ducks. particularly around the vent. The pigeon fly (hippoboscid fly. The sticktight flea. 6. 1960). often in groups. and subcutaneous tissue. The common human bedbug. This fly is unusual in that the larvae matures inside the female and pupates immediately upon ejection. 1997). may also attack poultry.. serve as intermediate hosts for Haemoproteus nettionis which infects domestic ducks in Canada. Biting midges. the fowl tick has been shown to transmit a number of spirochete. air sacs. louse fly). 1948. Ruff / Veterinary Parasitology 84 (1999) 337–347 341 importance of lice infestation is unclear. it is found in 60% of the layer systems in Denmark. Arachnids The northern fowl mite is the most ubiquitous and important ectoparasite of poultry (Arends. In turkeys. Other adult fleas of birds and mammals are intermittent feeders on poultry. but feed costs may increase by 1–6 cents per dozen eggs laid (Arends et al. The soft-bodied or fowl ticks of the genus Argas are the most important ticks in poultry although many species of hard ticks will feed intermittently on poultry.. Several other closely related species are found in the tropics and subtropics. 1950) to 15% (Glees and Raun. but common in breeder farms. . Dermanyssus gallinae. 1956). One other species deserves mention because of its economic impact and that is the larval chigger. Culicoides spp. only a few are generally of importance to parasitologists because they serve as intermediate hosts for other parasites. stable flies). often in large numbers which can have severe effects on production. Conversely. is found on a wide variety of birds and mammals. In addition. Although the chicken mite (red mite or roost mite). 1959) range. even when large numbers of lice were present. lice may be highly pathogenic in very young birds. 1984). Not only is egg production reduced by mites. Stockdale and Raun.2. other researchers report a decrease in egg production in the 11% (Edgar and King. This flea is unique among poultry fleas as the mouthparts are deeply embedded in the skin making the adults sessile. rickettsial. family Simuliidae.D.

1989). and/or mycotoxins can cause such imbalances (Ruff. 1978. and the reverse for histomoniasis. marked improvements in ventilation and nipple watering systems have improved litter conditions to where they are no longer favorable to the sporulation and survival of coccidial oocysts. by caging. As a result the level of exposure in modern broiler houses has become quite low. such as the regular removal of dead birds and restrictions on the movement of equipment and personnel also helps to reduce parasitic infections. followed by disinfection may have benefit when parasite numbers have become excessive. 1985) or the marked loss in pigment with chickens fed low levels of mycotoxin in the presence of very mild coccidiosis (Ruff and Wyatt. This also applies to some parasites that cross species such as turkeys as a reservoir for gapeworm in pheasants.342 M.1. Mild coccidiosis has been shown to interact with a variety of other disease agents both in the laboratory and the field. 1989). 1982). this takes the form of breaking the life cycle by preventing the bird from coming in contact with the intermediate or transport host.D. even when none of the infections are present at a severe enough level to produce significant effects by themselves. Good sanitation. For histomoniasis. 1956). infectious bronchitis virus. Effects with cryptosporidia are especially severe when the parasite is associated with other disease organisms such as infectious bronchitis virus and E. bacteria. Salmonella. Cleaning out contaminated litter. In general. physiological and immunological states (Ruff. 1993). 8. and numerous mycotoxins (reviewed by Ruff. Birds of different ages should not be raised in close proximity as older birds can serve as a reservoir for infection of young birds.. 1987). Control measures 8. Management Since effective medications are not available for many of the parasitic infections in poultry. faster growing broiler lines used today seem to be especially susceptible to minor imbalances in their nutritional. reovirus. The interactions are often quite striking as in the increase in leg problems in birds experiencing infection with low levels of E. or by reducing contact with the source of contamination. Huff and Ruff. However. the best control is by eliminating access of poultry to eggs of the cecal worms and earthworms. infectious bursal disease virus. The effects of these interactions can be measurable and economically significant. These include Clostridium. in the past 10 years. viruses. Marek’s disease virus. Interactions of low levels of parasites. such as feces. Ruff / Veterinary Parasitology 84 (1999) 337–347 7. Interactions have also been shown with nematodes and other infections. mitis and a mild reovirus (Ruff and Rosenberger. although they are not as dramatic as with the protozoa. Disease interactions The new. For many years it was assumed that management practices could do little to reduce coccidiosis because of the ability of the oocysts to survive for long periods and withstand most disinfectants used (Reid. . Control of earthworms in dirt-floor pens is often effective. coli (Current et al. Escherichia coli. management practices are about the only means left for control.

such as arprinocid. but to the industry as a whole. Judicious selection of an anticoccidial program is essential to slowing the development of resistance (McDougald and Reid. Sensitivity testing at moderate to high exposure levels is the only way to identify the resistance profile of an individual complex (Ruff and Danforth.M. If conditions change so that the exposure level rises.. The biggest problem associated with this control method is the development of resistance by the coccidia to all medications available for use. Capillaria. Prophylactic medication with anticoccidial drugs in the feed remains the major way of preventing coccidiosis (McDougald.D. The better the drug initially. 1989. Some excellent anticoccidials. the growth of the modern large-scale confinement poultry production facilities would not have been possible without the use of medications. but by 1989 82% of the isolates were resistant (Ruff. anthelmintics. 1990). 1996). Syngamus. 1986). a chemical in the starter feed an ionophore in the grower feed. such compounds were highly efficacious and inexpensive. the more likely poultry companies are to use it excessively.2. The use of shuttle programs (different medications within a growout period. 1982). 1994b). When first introduced. 1978) but by 1986 only onethird were sensitive (McDougald et al. nicarbazin during the fall and winter and a different medication in the spring and summer) both help to delay.. but have been taken off the market in US once again creating a potential hazard in isolated flocks. Chemotherapy Chemotherapy in the form of anticoccidials.e. Ruff (1994a) pointed out that in 1978 all field isolates tested were sensitive to monensin (Jeffers. In US. or were. The efficacy of modern anticoccidials is affected by the severity of exposure so some drugs. unpublished data). the latter under a minor use program. new compounds are lacking and none . No resistance was seen to halofuginone in 1982 (Mathis and McDougald. The nitroimidazoles (dimetridazole. are often not effective against the species of coccidia found in game birds (Ruff et al. Anticoccidials that are. or in some cases even avoid. ipronidazole. The remaining approved compounds have little efficacy. 1990). especially in relation to the dramatic results that were obtained. not only to individual production facilities. The tendency of the commercial poultry industry has been to use an effective drug continuously. McDougald and Reid. or ronidazole) are highly effective for control of histomoniasis. effective against Eimeria species of the chicken and turkey. Ruff / Veterinary Parasitology 84 (1999) 337–347 343 8. 1996). Even for these species. 1993. the appearance of resistance (McDougald. especially against coccidiosis. anthelmintics have been approved for only major nematodes such as the Ascaridia. 1990. will still work if exposure to coccidia is mild (Ruff and Danforth. have been removed from the market when wide spread resistance developed from overuse. Heterakis.. but can vary markedly between complexes (Ruff. Apparent efficacy at low levels of exposure in the field is not indicative of efficacy should the challenge increase. these drugs are often not able to control resistant populations of coccidia. The results have often been disastrous. Few drugs are available for treatment of helminth infections because the size of the market and severity of the problem does not justify the escalating cost of developing and obtaining regulatory approval for a new drug. and insecticides have been the mainstay for the prevention and control of parasitic infections in poultry. 1997). For example. Certainly.e. hoping that resistance will not develop. Such populations are generally consistent between farms that make up a broiler complex. 1997). i. and no medication in the finisher feed) or rotation between medications at different times of the year (i. such as the ionophores..

. especially when the infection is one such as coccidiosis that affects all stages of the nutrient utilization process (Ruff and Allen. 1993).3. This involves a complex interplay of internal factors including the levels and activity of cytokines. Immunity Vaccination is critical for the control of most bacterial and viral diseases in poultry. carbamates and synthetic pyrethroids. Initial attempts at vaccination to reduce the effects in commercial poultry operations used a live virulent vaccine. and the disease organism (Cook. leukocytes.D. mainly pyrethroids. 1997). and antigen presentation. tetramisole and disophenol. the immune system.S. There is increasing evidence that many of the recently developed lines of commercial poultry have been selected for maximum growth and feed efficiency at the expense of the ability to develop rapid and consistent immunity (Ruff. 1990). and thiabendazole are approved for use in poultry for control of the above species. coccidial infections can have adverse effects on viral or bacterial vaccination programs in poultry. Many different insecticides are available. should never be used on or around equipment. gutassociated lymphoid tissues. 1995). in breeders. organophosphates. only Hygromycin B. Klassing (1991) has reviewed the competition between the immune and production (growth) systems and the competition for nutrients. and even those have considerable restrictions. but especially piperazine. Few effective drugs have been identified for control of cestodes and trematodes and none are approved for use in poultry in the U. or other edible poultry products are of special concern so care must be used to follow label directions and withdrawal times. hexachloride. citarin. toxaphene. Coccivac (American Scientific Laboratories. These include bambendazole. piperazine. DE). macrophages. Ruff / Veterinary Parasitology 84 (1999) 337–347 are expected in the near future. Responding to a parasitic infection places added demands on the nutritional state which may be inadequate to generate the desired immune response. The ability of the host to limit the severity of a challenge infection is to a large part dependent on the ability to mount an immune response. chlordane. but immunity plays almost no role in the control of parasites except for coccidiosis. Drug resistance has been documented for all of these compounds. although fenbendazole and levamisole are effective (Reid and McDougald. fenbendazole. or feed ingredients. meat. Millsboro. In the latter disease. levamisole. Control of arthropod infestations is generally accomplished by the application of pesticides by dusting. or misting. aldrin. hormones. The live oocysts were introduced into the drinking water early in the bird’s life. 1989. Compounds such as DDT. Development of immunity depended on the successful cycling of low levels of coccidia in . 1997). benzene. poultry houses. Several other drugs have been reported to have efficacy in experimental infections against these and less common species of nematodes. 8. mebendazole. Residues in eggs. although highly effective. interest in immunity for prevention of economic losses is rising as drug resistance increases. Requirements for each of these methods are described by Arends (1982. pyrantel. In US. Thus. endrin or heptachlor. spraying. Users must check with the appropriate organization in their respective country to determine which are approved for use. feed. One of the major factors affecting the response of any animal to a vaccine or infection is the complex relationship among the nutritional state.344 M. More detail on use levels and times are given in Ruff and Norton (1997).

Proc. Y.J... Robertson.. Current.. but not complete. vaccines. the birds are not protected from wild strains while immunity is progressively induced by the developing and cycling parasites. Ruff / Veterinary Parasitology 84 (1999) 337–347 345 the litter to give a gradual. Vaccination with subunit vaccines continues to be a major area of research. pp. Sinha. C. 1984. North Carolina. (Eds.E. B. Ont. type of adjuvant.. Cook. 1998). Results have been more promising in battery type trials than in floor pen type experiments. but increasing. J. 33..R. 1457–1461.. Maryland Nut.. 1997. 1997). 1997. Ames. 289–296.B. Beard.. Recently. respectively.). Czech Republic). . Exposures that were too low or too high resulted in poor immunity or clinical disease with economic losses. Variables that affect results include the line of bird used. In: Calnek.W. parasite fraction. About 10 years ago. Arends. Upton. W. M. 16–22. McDougald..W.. Paracox (Schering-Plough Animal Health. immunity can be elicited against coccidial challenge (Danforth et al. are on the market in Europe and South America. Currently two live attenuated vaccines. Arends. Cryptosporidiosis. 1989. Research Institute of Biopharmacy and Verterinary Drugs. pp...L. M.. 703–704.M. Rockwood.H. W. the use of a gel to suspend the oocysts and give a very consistent dose of oocysts by ingestion of the gel has shown promise with the Immucox (Vetech Laboratories. J. H. Diseases of Poultry.J.. sp. 1993. 1997. 10th ed. Saif. Poultry Hlth. Y. Iowa. Haynes. Cryptosporidiidae) infecting chickens. should severe exposure to coccidia occur.L. J. and later by an eye spray at the hatchery (Danforth. & Process. Barnes. Iowa. and the targeted use of medications. 785–813.. (Apicomplexa. Indian Vet. Although these vaccines are highly successful in breeders where there is only a mild exposure to coccidia oocysts.. Iowa State University Press. References Ahmed. Ames. The life cycle of Cryptosporidium baileyi n.S.K. Control of other parasitic diseases will be based on the old method of breaking the life cycle and careful use of the few remaining antiparasitics. Use of this method was limited to protection of ‘heavy’ broilers. Prevalence of poultry helminthiasis in an arid-zone in Nigeria. L. North Carolina State University Extension Publishing. 70. Use is primarily in replacement and breeding flocks.J. 1982..R.). B. S. C. Mtg. J. Protozool. Diseases of Poultry. route and combinations of antigens.. Beard. L. J. 1986. Nutritional control of immune-induced depression of food intake and growth. 1993). 883–890. 10th ed.. or parasite products have demonstrated that partial. Immunization trials using antigens derived from recombinant proteins. pp. H. Thus. Nutrient modulation of the avian immune system. Canada) live vaccine (Danforth et al. Cook. Poultry Sci.I..J. the major disadvantage of such vaccines is that medication can not be used simultaneously. Middlesex. P. 63.M. T. pp. 6–13. C. External parasites and poultry pests. time of immunization. There has been considerable effort to develop live attenuated vaccines through the used of embryo passage of the coccidia or the selection of strains with an abbreviated life cycle (precocious lines). Current. In: Calnek. Danforth. Integrated Pest Management Manual. Iowa State University Press. 30th Nat. S. Arends. Impact of northern fowl mite on broiler breeder flocks in North Carolina.E. 1995. improvements in consistency of the initial dose to individual chicks were made by spraying the oocysts to the feed instead of in the water. Saif. Barnes.W. exposure.J.W. Payne. Future control of coccidiosis may well involve an integrated program involving management practices.M. but results to date have not yet yielded a commercial product... Raleigh.. Conf. Proc. McDougald. M.D. Prague. UK) and Livacox (Biopharm.J. (Eds.

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