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    TOXICOLOGICAL EVALUATION OF CERTAIN FOOD ADDITIVES



    WHO FOOD ADDITIVES SERIES 10





    The evaluations contained in this document were prepared by the
    Joint FAO/WHO Expert Committee on Food Additives*
    Rome, 21-29 April 1976



    Food and Agriculture Organization of the United Nations

    World Health Organization




    *Twentieth Report of the Joint FAO/WHO Expert Committee on Food
    Additives, Geneva, 1976, WHO Technical Report Series No. 599, FAO Food
    and Nutrition Series No. 1.

    NATAMYCIN (PIMORICIN (R))

    Explanation

         This substance has been evaluated for acceptable daily intake for
    man by the Joint FAO/WHO Expert Committee on Food Additives in 1968
    (see Annex I, Ref. 17, p. 27).

         Since the previous evaluation, additional data have become
    available and are summarized and discussed in the following monograph.
    Previously published monograph has been expanded and is reproduced in
    its entirety below.

    BIOLOGICAL DATA

    BIOCHEMICAL ASPECTS

         Little information is available on the absorption, distribution,
    excretion or metabolism of pimaricin in the body. No pimaricin (less
    than 1 µg/ml) could be detected in the blood following ingestion of
    500 mg by human subjects (Anonymous, 1968) and this helps to
    substantiate the statement (Raab, 1972) that pimaricin is not absorbed
    from the gut in animals or man.

    TOXICOLOGICAL STUDIES

    Special studies on allergic effects

         No allergic sensitization occurred among 111 patients being
    treated with pimaricin for a variety of conditions (Gruyper, 1961,
    1964). No history of allergic reactions was found in 73 workers
    engaged for an average of 5 years in the manufacture of pimaricin. No
    allergic reactions were obtained in the 71 who were tested by
    cutaneous or intradermal challenge doses (Malten, 1967). Repeated
    patch tests on 102 patients with various forms of eczema failed to
    demonstrate any sensitizing potential with pimaricin (Malten, 1968).

    Special studies on degradation products

    (1)  Acute toxicity

         Recent studies indicate that similar breakdown products of
    pimaricin occur in simulated gastric juice, 0.5% citric acid and urine
    and it appears likely that breakdown products in stored apples

              

    1    Natamycin is the international nonproprietary name of this
    substance, hitherto referred to as pimaricin in the reports of the
    Expert Committee.

    resemble those produced in gastric juice. The breakdown products are
    tetraenes related to pimaricin, principally the aglycone dimerized
    and/or decarboxylated; whether these would be absorbed remains to be
    tested (Brik, 1975). Approximately 50% pimaricin is broken down in 1
    hour in simulated gastric juice and losses from the stomach of 33-43%
    and 0-31% respectively occurred in fasted and non-fasted rats
    (Morgenstern and Muskens, 1975).

                                                                        

    Treatment of 1% or 5%                    %          Mouse i.p. LD50
    suspension                          decomposition      mg/kg bw
                                                                        

    kept at pH 2.2 with citric acid         74             200
    kept at pH 6.3 in the dark              13             200-400
    kept at pH 6.3 in the light             80             400-600
    kept at pH 8.5 (NaOH)                    0             150-250
    kept at pH 8.5 (NaOH)                    5             450
    kept at pH 10.4 with soda              100             >800
    kept at pH 6.3 with 0.1% H2O2            9             200-400
    kept at pH 5.0 in UV light               0             170
    kept at pH 5.0 in UV light              50             200
                                                                        

                                                           (Ottens, 1965)

    (2)  Short-term studies

    Rat

         Groups of 15 male and 15 female rats were fed for 98 days on
    diets containing 5% water, 5% of 0.5% citric acid, 500 ppm pimaricin
    or 5% of a solution of acid degraded pimaricin (pimaricin suspended in
    0.5% citric acid until only 14% of the activity remained). No animals
    died and weight gain was unaffected by treatment and no adverse
    effects were seen in the results of haematological examination or
    determination of the absolute weights of the liver and kidneys. The
    minor differences in the relative organ weights were considered
    coincidental and not due to treatment. Microscopic examination of a
    wide range of organs failed to detect any injury due to pimaricin
    degradation products (Hutchison et al., 1966).

         Slices of cheese were treated with 0.05% and 5% suspensions of 
    pimaricin and left to dry at room temperature. The antimicrobial 
    activity of the two cheeses declined to less than 20% and 60-80%
    during the 3 weeks storage period before they were incorporated into
    rat diet, the final dietary pimaricin plus degraded pimaricin contents
    being 3.6 or 360 ppm. Groups of 15 or 30 male and 15 or 30 female rats

    received diet containing fresh cheese freshly dressed with 0, 0.05 and
    5.0% pimaricin or diet containing cheese dressed with 0, 0.05 and 5%
    suspensions and stored for 3 weeks. The test lasted 7 weeks. No 
    abnormalities which could be attributed to pimaricin degradation 
    products were found on examination of the behaviour, appearance,
    morbidity, mortality, food consumption, body-weight gains,
    haematological indices, liver function, organ weights and macro- and
    micro-pathology of the animals (Wieriks, 1966).

         Groups of 10 male and 10 female rats were fed for 3 months on
    diets containing the peel of apples which had been untreated, freshly  
    treated with pimaricin or treated with pimaricin and stored for 2-8
    weeks to allow degradation to take place. A similar experiment was set
    up in which sausage skins (untreated, freshly treated or stored with
    pimaricin) were fed to rats. The dosage of pimaricin and its     
    degradation products cannot be calculated but the apple-skin diet
    provided rats with approximately 0, 50 and 1250 times the human likely
    intake and the sausage skin diet approximately 0, 1000 and 25 000
    times the human intake. Some minor abnormalities were found but none
    of the findings, in relation to growth rate, mortality, haematological
    indices, serum enzymes, liver function, organ weights or gross and
    micropathological changes, could be attributed to the intake of
    pimaricin breakdown products (Wieriks, 1971).

    Special studies on microbial resistance

         Pimaricin is active against a wide range of mycotic organisms
    such as dermatophytes and other fungi, yeasts and yeast-like organisms
    (including strains pathogenic to man, animals and plants and
    saprophytic varieties). Standard tests show that it has no activity on
    bacteria or on actinomycetes. There is no evidence that mycotoxins-
    forming species are unusually resistant to pimaricin (Raab, 1972).

         No yeast or yeast-like organisms have yet been reported to show
    primary resistance to pimaricin although some dermatophytes are
    resistant to its activity.

         Compared with bacteria and antibiotics, it is difficult to induce
    resistance to pimaricin in yeasts (Khoudokmoff and Petru, 1974) and
    there was some evidence that the resistance which could be obtained
    was based on selection of naturally more resistant strains and not on
    adaptation. Resistant cultures showed reduced pathogenicity (Athar and
    Winner, 1971). No evidence of resistance in its clinical use has been
    recorded.

         Cross-resistance with other antimicrobials has been investigated.
    Amphotericin B exhibited cross-resistance with nystatin, filipin,
    endomycin and candidin but not pimaricin (Walter and Heilmeyer, 1969;
    Bodenhoff, 1968; Littman et al., 1958; Stout and Pagano, 1956).
    Nystatin and amphotericin B resistant organisms were susceptible to
    pimaricin (Sörensen et. al., 1959) and a wide selection of nystatin

    resistant yeasts also exhibited normal susceptibilities to pimaricin
    (Hejzlar and Vymola, 1970). More recent in vitro studies have
    established that cross-resistance between pimaricin and nystatin and
    amphotericin may occur (Athar and Winner, 1971).

    Special studies on mutagenicity

         Groups of 10 male rats taken from the second litters of the F1
    generation of a 3-generation reproduction study were fed on control
    diet until sexually mature when they received, by gastric intubation,
    0, 5, 15, 50 or 100 mg pimaricin/kg bw daily for 7 days. Each rat was
    mated each week for 8 consecutive weeks with 2 virgin untreated
    females. Each female was killed and examined 13 days after mating had
    taken place. No differences between control and test animals were
    found in relation to the numbers of implant sites, live and dead
    foetuses or the mutagenic index (Cox et al., 1973).

         Five males and 5 females were selected at random from the five
    litters produced in a 3-generation study in which animals were fed on
    diets providing 0, 5, 15, 50 or 100 mg pimaricin/kg bw/day. Three to 4
    hours before sacrifice the animals were administered colchicine and a
    bone marrow preparation was made for examination for aberrant
    chromatin material. The number of abnormalities in the metaphase
    chromosomal preparations of test groups did not suffer significantly
    from the number occurring in sham-treated controls (Cox et al., 1973).

    Special studies on reproduction

         Groups of 10 females and 5 males receiving 0 or 1000 ppm
    pimaricin in their diet were mated after 181 and 223 days on the test.
    Other groups were mated after 48, 174 and 250 days on the diets; 4
    control and 4 test female young from the second mating of this study
    were fed on the same diet as their parents and mated when 107 days of
    age. The pups from pimaricin-treated animals had lower mean body-
    weights at weaning than control pups but examination of the results of
    the 54 matings showed that their fertility, gestation, lactation and
    viability indices were similar to or better than the controls. There
    was a low incidence of abnormalities among pups in this study and no
    abnormality could be attributed to pimaricin treatment (Levinskas,
    1966; Levinskas et al., 1963).

         Groups of 10 male and 20 female rats were fed on diet providing 0
    (two groups), 5, 15, 50 or 100 mg pimaricin/kg bw/day for 11 weeks.
    These formed generation F0 of a 3-generation reproduction study, with
    2 litters being produced in each generation. In the 100 mg/kg group
    there was an increased number of foetuses born dead, a decrease in the
    number born alive and a decrease in the number surviving at 21 days.
    Pup weight was depressed in the second litters of the F0 and F1
    generations and both litters of the F2 generation. However, the

    fertility, gestation, viability and lactation indices were within
    normal limits for both litters of all 3 generations. The 5, 15 and
    50 mg/kg dosage levels had no detectable effect on growth or
    reproduction (Cox et al., 1973).

    Special studies on teratogenicity

         Groups of 20 female rats from the second litters of generation F1
    of a 3-generation study on pimaricin were reared to maturity on
    control diet and mated with untreated males. The females were given by
    gastric intubation the same dose level of pimaricin as their parents
    (0, 5, 15, 50 or 100 mg pimaricin/kg bw/day) during the 6-15 days of
    pregnancy. They were killed and examined on the 20th day of pregnancy.
    No differences between control and test animals were seen in relation
    to the number of pregnancies, live letters, implant sites, resorption
    sites, live and dead foetuses or skeletal and soft tissue
    abnormalities (Cox et al. 1973).

         Groups of 10-12 female rabbits were administered 0, 5, 15 or
    50 mg pimaricin/kg bw/day by gavage on the 6-18th days of pregnancy.
    They were examined on the 29th day and the numbers of corpora lutea,
    implantation sites, resorption sites and live and dead foetuses
    recorded. No adverse effects of pimaricin on nidation or maternal or
    foetal survival were found. The number of abnormalities seen in the
    soft or skeletal tissues did not differ from the number occurring
    spontaneously in controls (Bailey and Morgareidge, 1974).

    Acute toxicity

                                                                        

                                        LD50
    Animal        Sex        Route     mg/kg bw    Reference
                                                                        

    Mouse         -          oral       1 500      Anonymous, 1965
                  -          oral       2 500      Anonymous, 1965

    Rat           male       oral       2 730      Levinskas et al., 1966
                  female     oral       4 670      Levinskas et al., 1966

    Guinea-pig    female     oral         450      Struyk et al., 1958

    Rabbit        male       oral       1 420      Levinskas et al., 1966

    Dog           -          oral       1 000      Anonymous, 1965
                                                                        

         In rabbits a dose of 500 mg/kg and above caused diarrhoea and
    animals which died had a haemorrhagic gastric mucosa. Raab (1972)
    reports that pimaricin complexed with one-third its weight of a
    modified polysaccharide increases its toxicity sixfold and that when
    fed to rats pimaricin could be detected in blood.

    Short-term studies

    Rat

         Oral administration of 50-70 mg pimaricin/kg bw daily for 5-10
    weeks had no effect on the growth, blood or tissues of rats. A daily
    oral dose of 150 mg/kg for 9 weeks caused some growth inhibition and a
    daily dose of 500 mg/kg caused 30% of the rats to die within 2 weeks
    (Struyk, 1958).

         Groups of 20 male and 20 female rats were fed on diets containing
    0, 125, 500, 2000 or 8000 ppm pimaricin for 94-96 days. None of the 5
    deaths could be attributed to treatment. Growth was retarded and food
    intake was diminished at the 2 highest dosage levels. The results of
    haematological examinations and organ weights were within normal
    limits and no gross or microscopic lesions could be attributed to
    pimaricin intake (Levinskas et al., 1966).

    Dog

         Pimaricin was fed to groups of 3 male and 3 female beagle dogs at
    dietary levels of 0, 125, 250 or 500 ppm for 2 years. All but one dog,
    receiving 250 ppm diet, survived for 2 years; the death was unrelated
    to exposure to pimaricin. No effect was seen on food intake but males
    receiving the 500 ppm diet did not grow as rapidly as controls
    initially and after 15 months when the dietary intake was reduced some
    animals were unable to maintain a satisfactory body-weight. Results of
    haematological examinations and clinical chemical studies revealed no
    abnormalities. No effects of significance were found on determination
    of organ weights or on gross and microscopic examination for
    pathological changes (Levinskas et al., 1966).

    Long-term studies

    Rat

         Groups of 35-40 male and 35-40 female rats received diet
    containing 0, 125, 250, 500 and 1000 ppm pimaricin for 2 years.
    Animals remained in good health and their survival was unaffected by
    pimaricin. Inhibition of growth rate and a diminished food intake
    occurred in both sexes receiving the 1000 ppm diet but lower dosage
    levels had no adverse effects. The results of haematological
    investigations and determination of organ weights and the gross and
    microscopic pathology showed no differences between treated and

    control groups. The number and types of tumours found in pimaricin-
    treated rats were not significantly different from untreated animals
    (Levinskas et al., 1966).

    OBSERVATIONS IN MAN

         In man nausea, vomiting and diarrhoea have occasionally been
    caused by oral doses of 300-400 mg pimaricin daily; no changes in
    peripheral blood have been observed (Royal Netherlands Fermentation
    Industries, 1966). In a group of 10 patients with systemic mycoses who
    received oral doses of 50-1000 mg/day for 13-180 days, nausea,
    vomiting and diarrhoea occurred in those receiving 600-1000 mg/day
    (Newcomer et al., 1960).

    Comments

         Information available on the metabolism of pimaricin suggests it
    is not absorbed to a significant extent from the gastrointestinal
    tract. The only adverse effects found in animal studies were a
    decrease in food intake with a decrease in the rate of body-weight
    gain. The dog appeared to be more sensitive than the rat, the response
    appearing in dogs with doses of the order of 10 mg/kg/day. In man mild
    gastrointestinal symptoms begin to appear at daily dosage levels of
    about 5 mg/kg, although much higher dosage levels have been taken
    without ill-effects being observed. Adequate studies have demonstrated
    no adverse effects on reproduction nor any carcinogenic, mutagenic or
    teratogenic potential. Work on the composition of breakdown products
    suggests that those formed in food are likely to be the same as those
    formed in acid conditions in the stomach; the feeding studies carried
    out on pimaricin are therefore relevant to breakdown products. Studies
    in rats on food containing breakdown products or citric acid degraded
    pimaricin also suggest no adverse effects are likely from the
    breakdown of pimaricin. Although widely used there are no reports of
    allergic reactions. Despite general reservations concerning the use as
    food additives of therapeutically useful antimicrobial substances, the
    Committee agreed that data demonstrated that problems related to the
    development of clinically significant microbial resistance or cross-
    resistance were unlikely to occur with pimaricin (see Appendix 4 of
    the 20th Report).

    EVALUATION

    Level causing no toxicological effects

         Rat - 500 ppm in diet, equivalent to 25 mg/kg bw
         Dog - 250 ppm in diet, equivalent to 6 mg/kg bw
         Man - approximately 200 mg/man/day, equivalent to 3 mg/kg bw

    Estimate of acceptable daily intake for man

         0-0.3 mg/kg bw

    REFERENCES

    Anonymous (1965) Data on the safety of the use of pimaricin as
         preservative against mold growth on cheese. Summary of the
         results of acute and chronic toxicity tests. Unpublished report
         from Royal Netherlands Fermentation Industries Ltd, Delft, The
         Netherlands, submitted to the World Health Organization

    Anonymous (1968) Absorption of pimaricin following oral
         administration. Unpublished report from Royal Netherlands
         Fermentation Industries Ltd, submitted to the World Health
         Organization

    Athar, M. A. and Winner, H. I. (1971) The development of resistance by
         Candida species to polyene antibiotics in vitro, J. Med.
         Microbiol., 4, 505-517

    Bailey, D. E. and Morgareidge, K. (1974) Teratogenicity test with
         pimaricin. Unpublished report (No. 1-1052) from Food and Drug
         Research Laboratories Inc., submitted to the World Health
         Organization

    Bodenhoff, J. (1968) Resistenzuntersuchungen von Candida albicans, mit
         besonderer Berücksichtigung von zwei während einer längeren Zeit
         mittels antibiotica behandelten Patienten, Scand. Dent. J.,
         76, 279

    Brik, H. (1975) Natamycin (pimaricin). New high-molecular
         decomposition products with intact lactone-ring. Unpublished
         report submitted to the World Health Organization by Gist-
         Brocades NV, Delft, The Netherlands

    Cox, G. E., Bailey, D. E. and Morgareidge, K. (1973) Unpublished
         report (No. 1-1052) from Food and Drug Research Laboratories
         Inc., submitted to the World Health Organization

    Grupper, Ch. (1961) Personal communication from the Hōpital Saint-
         Louis, Paris

    Grupper, Ch. (1964) Pimaricin in the treatment of superficial
         mucocutaneous monoliasis. Intern. Congr. Trop. Dermat. Naples,
         June 1964

    Hejzlar, M. and Vymola, F. (1970) Comparative study of pimaricin and
         fungicidin activity in vitro, J. Hyg. Epidem. (Praha), 14,
         211

    Hutchison, E. B., Ribelin, W. E. and Levinskas, G. J. (1966) 98-day
         study in the rat. Unpublished report by American Cyanamid Co.,
         submitted to the World Health Organization

    Khandokormoff, B. and Petru, M. (1974) On the possible development of
         antibiotic resistance amongst fungi with special reference to the
         use of pimaricin as a preservative in the food industry.
         Unpublished report from Gist-Brocades NV, Research and
         Development Division, Delft, The Netherlands, submitted to the
         World Health Organization

    Levinskas, G. J., Shaffer, C. B., Bushey, C., Kinde, M. L.,
         Stackhouse, D. W. and Vidone, L. B. (1963) Two-year feeding to
         rats. Unpublished report from the Central Medical Dept., American
         Cyanamid Co., submitted to the World Health Organization

    Levinskas, G. J., Ribelin, W. E. and Shaffer, C. B. (1966) Acute and
         chronic toxicity of pimaricin, Tox. and Appl. Pharmacol., 8,
         97-109

    Littman, M. L., Pisano, M. A. and Lancaster, R. M. (1958) Induced
         resistance of Candida species to nystatin and amphoteracin B. In:
         Antibiotics Ann.: 981. Medical Encyclopedia, New York, NY

    Malten, K. E. (1967) Report of an investigation concerning possible
         allergic side effects of pimaricin in humans. Unpublished report
         from the Instituut voor Geneeskunde en Maatschappij, Nijmegen,
         The Netherlands, submitted to the World Health Organization by
         Gist-Brocades NV, Delft, The Netherlands

    Malten, K. E. (1968) Report on investigation into possible sensitising
         side effects of pimaricin in human beings. Unpublished report
         from the Instituut voor Geneeskunde en Maatschappij, Nijmegen,
         submitted to the World Health Organization by Gist-Brocades NV,
         Delft, The Netherlands

    Morgenstern, A. P. and Muskens, G. J. A. M. (1975) Further data on the
         toxicity of the decomposition products of pimaricin. Unpublished
         report submitted to the World Health Organization by Gist-
         Brocades NV, Delft, The Netherlands

    Newcomer, V. D., Sternberg, T. H., Wright, E. T., Reisner, R. M.,
         McNall, E.G. and Sorensin, L. J. (1960) The treatment of systemic
         diseases with orally administered pimaricin: Preliminary report,
         Ann. N.Y. Acad Sci., 89, 240-246

    Ottens, H. (1965) Unpublished report submitted to the World Health
         Organization by Royal Netherlands Fermentation Industries, Delft,
         The Netherlands

    Raab, W. P. (1972) Natamycin (pimaricin). Its properties and
         possibilities in medicine. Georg Thieme Publishers, Stuttgart

    Sörensen, L. J., McNall, E.G. and Sternberg, T. H. (1959) The
         development of strains of Candida albicans and Coccidioides
         immitis which are resistant to amphotericin B. In: Antibiotics
         Ann.: 920-923. Medical Encyclopedia, New York, NY

    Stout, H. A. and Pagano, J. F. (1956) Resistance studies with
         nystatin. In: Antibiotics Ann.: 704. New York, NY

    Struyk, A. P., Hoette, I., Drost, G., Waisvisz, J. M., van Eek, T. and
         Hoogerheide, J. C. (1958) Pimaricin, a new antifungal antibiotic.
         In: Antibiotics Annual 1957-1958 (H. Welch and F. Marti-Ibanez,
         eds.), pp. 878-885. Medical Encylopedia, Inc., New York

    Walter, A.M. and Heilmeyer, L. (1969) Antibiotika Fibel. Thieme
         Verlag, Stuttgart

    Wieriks, J. (1966) Pimaricin in cheese: a toxicity test of seven weeks
         in rats. Unpublished report from the KNGSF-Research of the Royal
         Netherlands Fermentation Industries Ltd, submitted to the World
         Health Organization

    Wieriks, J. (1971) Pimaricin in apples: a toxicity test of three
         months in rats. Unpublished report from the Royal Netherlands
         Fermentation Industries Ltd, submitted to the World Health
         Organization


    See Also:
       Toxicological Abbreviations