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Studies of Coproporphyrin. Ii. an Investigation of The

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Studies of Coproporphyrin. Ii. an Investigation of The STUDIES OF COPROPORPHYRIN. II. AN INVESTIGATION OF THE CONTRIBUTION TO THE URINARY COPROPORPHYRIN OF HEMOGLOBIN AND OF BACTERIAL METABOLISM IN THE INTESTINAL TRACT 1, 2 By EVREL A. LARSON AND CECIL JAMES WATSON (From the Department of Medicine, University of Minnesota Hospital, Minneapolis) (Received for publication July 9, 1948) Stokvis (1) advanced the idea that blood in had previously shown that hemoglobin is converted the intestinal tract was the source of the urinary in small part to protoporphyrin in the colon, and porphyrin. Schumm (2) also held this belief. Sub- Kammerer (16) ascribed its formation to a sym- sequent studies, notably those of Fischer and Hil- biotic activity of the bacterial flora. Hill and mer (3), Brugsch (4, 5), and Kaunitz (6) indi- Holden (17) showed, however, that pure cul- cated that a variable fraction of the urinary copro- tures of E. coli liberated free protoporphyrin from porphyrin was thus derived. The presence of a hemoglobin; this was confirmed by van den Bergh porphyrin in meconium (2, 7, 8), later identified and co-workers (18). No direct evidence has by Waldenstr6m as coproporphyrin I (9), to- been described, however, for the intestinal forma- gether with a number of other evidences of an en- tion of coproporphyrin III from hemoglobin, al- dogenous formation, which are discussed in de- though the above-mentioned work of Jakob's sug- tail in recent reviews- (10, 11), have made it rea- gested that this might take place. In a previous sonably clear that at most not more than a certain study (19), it was shown that in the presence of fraction of the, urinary coproporphyrin (UCP) complete biliary obstruction due to cancer, copro- could be regarded as originating in the intestinal porphyrin could not be demonstrated in the acholic tract. The purpose of the present investigation feces even when there was bleeding into the upper was to obtain more definite information as to the gastrointestinal tract. This observation does not size of this fraction, under various experimental favor an origin from hemoglobin in the bowel, but and clinical conditions. It was also determined the possibility could not be excluded that copro- to study the relative percentage of coproporphyrin porphyrin thus formed had been entirely reab- isomers composing any increases which might be sorbed. observed, since previous studies bearing on these (2) A formation of coproporphyrin, either I questions had dealt only with the total copro- or III, as an independent bacterial synthesis in porphyrin. It was conceivable on a priori reason- the absence of hemoglobin. Fischer and co-work- ing, that any one or a combination of the following ers (3, 20) demonstrated that yeast cells under- might alter the total coproporphyrin concentration going autolysis, synthesize coproporphyrin I. or the isomer distribution in the urine: Kench and Wilkinson (21) have recently shown (1) A formation of coproporphyrin III from that yeast cells elaborate both isomers, the pre- hemoglobin, by the bacterial flora of the colon, ponderance depending on the conditions of the with reabsorption and excretion in the urine. culture. Coulter and Stone (22) found that diph- showed that pure cultures of E. coli theria bacilli in broth cultures form coproporphyrin Jakob (12) in an amount roughly proportional to that of the produce small amounts of coproporphyrin III in Snapper toxin produced. Gray and Holt (23) have re- the presence of hemoglobin. (13-15) cently demonstrated that this is the type III iso- 'Aided by grants from the John and Mary R. Markle mer and that it is formed in relatively large amount Foundation, New York City, and the Medical Research under suitable conditions of growth. All of these Fund of the Graduate School, University of Minnesota, observations suggested that the bacterial flora of Minneapolis. 2A portion of this study was included in a thesis sub- the human colon might, at least under certain cir- mitted (by E. A. L.) in partial fulfillment of the require- cumstances, produce either coproporphyrin I or ments for the Ph.D. degree, University of Minnesota. III, and, if it were absorbed, might thus bring 452 STUDIES OF COPROPORPHYRIN. II. 453 about an increased urinary excretion of the corre- the increases which he noted were composed of sponding isomer. von Mallinkrodt-Haupt (24) has, type III isomer, derived from the fed hemoglobin. in fact, postulated that the urinary coproporphyrin Kaunitz (6) and Boas (25, 26) described increases is wholly related to the bacterial flora in the colon, of urinary coproporphyrin following gastrointes- and that the increases described in pernicious ane- tinal bleeding due to peptic ulcer or malignancy. mia are related to the effect of achylia in altering This increase was likewise assumed to be composed the flora. It will be seen subsequently that the evi- of the type III isomer, although it was not iso- dence in favor of this theory is indeed very meager. lated. There is also the possibility that some de- (3) The further possibility had to be considered gree of liver functional impairment had occurred that liver function plays an important role with re- with resultant increase of type I rather than type spect to coproporphyrin I or III, which might orig- III, an association which has been discussed pre- inate in the intestinal tract whether from hemo- viously (11), and in favor of which there is abun- globin or bacterial metabolism. Kaunitz' study dant evidence in the literature (5, 10, 27-29). It (6) suggested that coproporphyrin is absorbed seems less probable, however, that this factor from the intestine but that it does not appear in the would be important after the simple ingestion of urine in appreciable amount unless there is as- blood by normal individuals, which was reported sociated liver functional impairment. Thus, after by Schumm (2), and Fischer (3) to be followed oral administration of 20 Gm. doses of crystal- by an increased urinary coproporphyrin of un- line hemoglobin, significant increases of urinary determined type. This was not confirmed by other coproporphyrin were observed only in cases of investigators (14, 15, 30, 31), nor were Borst and liver disease, or in instances where liver injury K6nigsd6rffer (32) able to detect the appearance was postulated as a result of severe anemia or of any porphyrin in the blood plasma after in- toxemia. Kaunitz assumed but did not prove that gestion of coproporphyrin. Gamma/Day 40 Copro --- - Urine 20 | 2 Oay Periods 40 Copro 20 I 1. -I I 100 - Proto so0 60 Feces Day Periods 60 Deu tecro so 20I -L Urobil inogen 15 Mgm/day I 4 8 12 16 20 Days FIG. 1. NORMAL EXCRETION OF PORPHYRIN IN DoGs Dog No. 1: Solid lines; diet-milk. Dog No. 2: Broken lines; diet-"kibbled" dog food and milk. 454 EVREL A. LARSON AND CECIL JAMES WATSON MATERIAL AND METHODS The method used for determining coproporphyrin in the In view of the above considerations, the present study urine, both total and isomer distribution, was that of in Schwartz and co-workers (33). The method for the was planned as outlined the following: feces was that described by Watson and Layne (34). I. Studies on dogs. This is not an exact procedure but permits a rough A. Feeding of blood-two dogs. approximation of the three main types of porphyrins B. Feeding of raw meat-two dogs. found in the feces: 1) coproporphyrin, 2) protoporphyrin, II. Studies on human subjects. 3) deutero- and the pseudo-deuteroporphyrins (19). The A. Cases hating blood in the gastrointestinal tract animals used were shepherd dogs, weighing 20-30 pounds, due either to hemorrhage or to feeding of housed in standard metabolism cages which were so con- blood: structed that the urine could be collected quantitatively Hemorrhagic gastritis, one case; malnutrition, under a small amount of toluene preservative. During one case; hepatic gumma, one case; bacterial the control period, one dog was maintained on a strict endocarditis, one case; cholecystitis and chole- milk diet, productive of marked constipation, the other on lithiasis, three cases; infectious hepatitis (re- a diet of "kibbled dog food" and milk, with which the covery phase), one case; carcinoma of head of bowel movements were normal. The urine coproporphy- pancreas, one case; cirrhosis and chronic al- rin determination was carried out every two days. As coholism, two cases; idiopathic cirrhosis, one mentioned previously, coproporphyrin does not deteriorate case. significantly in this period of time. In the human experi- B. Feeding of crystalline coproporphyrins: ments determinations were made on 24 hour samples of 1) Type III isomer-3-5 mgm. orally. urine. The feces porphyrins in both dogs and humans Bacterial endocarditis, one case; cholecystitis were determined on four-day collections. Urobilinogen and cholelithiasis, one case; acute alcohol- was determined by Watson's modification (35) of Ter- ism, one case; active duodenal ulcer with- wens method (36). Porphyrin isolations and melting out hemorrhage, one case; cirrhosis and point determinations were carried out according to pre- chronic alcoholism, one case. viously described methods (19, 37, 38, 39). The total 2) Type I isomer-3 mgm. orally. heme pigments of the feces were determined by the Cirrhosis and chronic alcoholism, one case. method of Flink and Watson (40). The crystalline Diet Diet Gamma/Day "Kibbled" Dog Food Mi lk and Milk 75 Copro 50 F Urine 25 Imimiru 2 Day Periods 100 - Copro 75 CHICI 50 25- -I 120 Proto 90 60 - 30 - t i i i -4 - feces 80- 4 Day Periods Deutero 60- 40- .. I 20 - Hemochromogenf I _ _ 15 a --. Urobilinogen 10 - Mgm/day 4 8 12 20 4 8 12 Days FIG. 2. EFFECT OF DIETARY CHANGE UPON THE PORPHYRIN EXCRETION Dog No.
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