FIBROCYSTIC DISEASE OF THE PANCREAS: STUDY OF FOURTEEN. Section on Pathologic A nalomy. Section on Pediatrics Mayo Clinic, Rochester, Minnesota
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1 FIBROCYSTIC DISEASE OF THE PANCREAS: STUDY OF FOURTEEN CASES* During the last decade and particularly during the last five years, largely as a result of the studies of Andersen 1, much attention has been focused on the condition known as fibrocystic disease of the pancreas. Over a period of eighteen years, this condition has been observed at necropsy in fourteen cases at the Mayo Clinic. Ten of these patients were males and four were females. Their mean age at the time of death was 8.7 months. CLASSIFICATION BY A. H. BAGGENSTOSS, M.D. Section on Pathologic A nalomy AND R. L. J. KENNEDY, M.D. Although the clinical picture varied considerably, the cases may be classified into the three fairly distinct groups first delineated by Andersen. The first group includes patients who die during the first week or two of life because of meconium ileus, intestinal stenosis or atresia. Only one patient in our series belonged to this group.' This was a male infant, five days old, who died of meconium ileus. The second group includes patients who present symptoms referable either to the respiratory system or to the gastro-intestinal tract and who die usually during the first year of life. Eight patients in our series belonged to this group. In our experience, the predominant signs and symptoms were the result of pulmonary infection. Coughing, which was practically always present, sometimes was described as dry and brassy and at other times as spasmodic and productive. The cough frequently is similar to the cough of pertussis. Cyanosis, particularly in the terminal stage, often is present. Three of the eight patients presented no symptoms referable to the gastro-intestinal tract. Three patients had feeding and nutritional problems and only two had diarrhea. All eight patients died as a result of infection of the respiratory tract. The mean age at the time of death was 7.4 months. The following is an illustrative case: * Read before the Twenty-Third Annual Meeting of the American Society of Clinical Pathologists, Chicago, June 9, Section on Pediatrics Mayo Clinic, Rochester, Minnesota 64 A male infant, two months of age, had three healthy siblings. Five other siblings, who had died before they attained the age of five months, had had a constant cough that began shortly after birth and also diarrhea. When the patient was two weeks of age, a constant cough developed and, as in the case of his siblings, this was suspected of being due to pertussis. By the time he was two months of age, the stools had become loose and resembled those characteristic of celiac disease. Our attention was focused chiefly on the condition of the lungs. Roentgenograms showed a condition at the base of the right lung that was thought to be pneumonitis. Respiration was difficult apparently because of some obstruction. Bronchoscopic examination revealed thick tenacious pus in the bronchial tree. The patient's course was rapidly downhill. Death was thought to be attributable primarily to pneumonia. The third group includes patients who have many symptoms and signs of celiac disease such as intolerance to fats and carbohydrates; large, foamy, light-colored and foul-smelling stools and failure to gain in weight and height. Unlike patients who have celiac disease, however, these patients also suffer from chronic bronchitis and bronchiectasis. They do not improve on accepted dietary treatment for celiac disease. Trypsin in the duodenal contents is reduced in amount or absent. Five patients in our series belonged to this group. They all died as a result of pulmonary infection. The mean age at the time of death was fourteen months. The following is an illustrative case: A male infant, ten months of age, had weighed 5 pounds, 12 ounces (2.6 kg.) at the time of delivery by cesarean section. A mild cough always had been present. When the patient was five months old, a diagnosis of atelectasis of the right lung had been made elsewhere. The stools had been foul and copious but not particularly fatty. He had been hospitalized a number of times because of cough and fever. On examination at the clinic he was emaciated and dehydrated. The abdomen was distended and gluteal fat was absent. Assay of duodenal contents revealed only a third of the normal amount of trypsin. The diag-
2 FIBROCYSTIC DISEASE OF PANCREAS 65 nosis was fibrocystic disease of the pancreas and bronchitis. The patient failed rapidly. Convulsions developed and death occurred five days after admission. PATHOLOGIC ANATOMY Pancreas. The pancreas presents few grossly recognizable changes. Some investigators have described infiltration with fat and increase in fibrous connective tissue between the lobules. The lobules have been described as rounded and uneven in size. Occasionally a grating sound has been noted as the knife passed through calciwhichin our'cases.varied considerably, apparently is dependent on the developmental stage of the disease (figs. 1 and 2). Certain features were common to all cases. Dilated ducts and acini contained varying amounts of coagulated secretion. The cells of the epithelial lining were flattened but only rarely were squamous in type. The secreted material occasionally had a laminated appearance and usually it was acidophilic. The intra-acihar material stained like mucus and occasionally like fibrin when appropriate stains were used. This suggests that the material is a FIG. 1. FJBROCYSTIC DISEASE OF THE PANCREAS a, early stage; slight dilatation of acini and ducts and slight increase in connective tissue (X90); b, moderately advanced stage. Note the inspissated secretion (X105). fied concretions. In some of our cases, the gland appeared to be firmer than normal and contained tiny opaque' grayish-yellow nodules. The main pancreatic duct has been patent in most reported cases. In our own cases, this duct could not be followed with a probe throughout its extent, but, according to Andersen, with whom we agree, this is not proof of the presence of obstruction in view of the small size of the duct in infants and young children. The fact that no part of the duct ever was found to be dilated is also evidence against obstruction. The histologic appearance of the pancreas, mucoprotein of some type but determination of the exact composition awaits careful chemical analysis. There was atrophy of the acinar parenchyma and variable increase in interacinar and interlobular connective tissue. A few lymphocytes and mononuclear cells were observed in the interstitial tissue but the predominant cell was the fibroblast. In the earliest stage of the disease, the acini and ducts were dilated only slightly and only slight increase in the interacinar connective tissue was present. These findings were demonstrated in the case of an infant who at death was only
3 66 A. H. BAGGENSTOSS AND R. L. J. KENNEDY eleven weeks of age (fig. la). A moderately advanced stage is presented in figure 16. The most advanced stage, histologically speaking, that was observed in our cases is shown in figure 2a. The patient had been twenty-one months of age a t the time of death. The islands of Langerhans usually are described as normal in appearance. In twelve of our fourteen cases, however, slight but definite abnormalities in histologic structure were observed. In most cases, the cells were loosely arranged in in which the patients died of disease of the respiratory tract. Formation of abscesses with organization of the exudate by fibroblasts occurred in twelve cases (fig. 36). Organization, however, was usually of slight degree. Cultures of the bronchial exudate and abscesses as a rule revealed the presence of Staphylococcus aureus. Squamatization or so-called metaplasia of the bronchial epithelium was present in seven cases (fig. 4). Liver. Fatty metamorphosis of the liver, which frequently has been described in the literature, FIG. 2. FIBROCYSTIC DISEASE OF THE PANCREAS a, advanced stage; parenchyma has been largely replaced by fibrous connective tissue and only a few dilated ducts and acini are present (X110); b, islands of Langerhans. Note loose arrangement of cells; presumably a result of intercellular edema (XI15). bands and in a few cases intercellular edema was present (fig. 26). Lungs. The gross pulmonary lesions consisted of suppurative bronchitis and bronchiectasis, patches of bronchopneumonia and abscesses (fig. 3a). Hyperexpansion of portions of the lungs was a frequent finding. The bronchi usually contained mucopurulent exudates that were unusually thick and tenacious. Histologically, suppurative bronchitis and bronchiolitis with ulceration of the mucous membrane and bronchiectasis, as well as more recent bronchopneumonia, was a feature in all thirteen cases was present in seven cases. The degree of fatty change was mild in four cases, moderate in two cases and severe in one case. Chronic passive congestion of moderate degree occurred in three cases. In two of these cases, atrophy with central necrosis was present. Gastro-intestinal tract. Distention of the glands of the duodenum with mucus was observed in nine cases. In three cases, this distention involved only the mucosal glands (fig. 5a), and in one case only Brunner's glands (fig. 56). In five cases both types of glands were affected. No similar changes were observed in any other portion
4 'FIG. 3a. Cut surface of lung; suppurative bronchitis, bronchiectasis, abscesses and bronchopneumonia; b, abscess formation with early organization of the exudate (X115). FIG. 4a. Bronchiectasis; note squamatization of bronchial epithelium and peribronchitis (X80); b, squamatization of bronchial epithelium (X260). 67
5 F I G. 5a. Mucosal glands of duodenum distended with mucus (XSO); b, Brunner's glands distended with mucus (X80). FIG. 6. DEPOSITS OF CALCIUM SALTS I N R E N A L TUBULES AND EPITHELIAL CELLS (X110) 68
6 FIBROCYSTIC DISEASE OF PANCREAS 69 of the gastro-intestinal tract. Atrophy of the mucosa of the ileum and jejunum occasionally was observed. Kidney. Calcium salts were present in the cells of the convoluted tubules, in Henle's loops and occasionally in the cells of the collecting tubules (fig. 6). Calcium salts in small amounts were found in seven cases, in moderate amounts in five cases and in large amounts in two cases. The exact significance of the presence of calcium is unknown but it may be indicative of some disturbance in metabolism or excretion. No other significant renal abnormalities were noted. ETIOLOGY The underlying cause of fibrocystic disease of the pancreas is unknown. The presence of the condition in the newborn and its early development in infants has suggested to many investigators the possibility that the basic abnormality is congenital. The tendency for fibrocystic disease to occur in more than one member of a family also favors the hypothesis that it is of congenital origin. In the first illustrative case report in this paper, five siblings of the patient had died before attaining the age of five months. In each instance, a constant cough and diarrhea had developed shortly after birth. The patient also had three healthy siblings. In another case two siblings were living and well and one sibling had died of fibrocystic disease of the pancreas. In a third case the only sister, who was three years old, also had symptoms of fibrocystic disease. Eight patients in our series had no siblings. In three cases the siblings were all living and well at the time of death of the patient. The majority of cases of fibrocystic disease that have been reported in the literature have been single instances in a family. Obstruction of the pancreatic ducts is one of the most likely causes of fibrocystic disease. Rauch, Litvak and Steiner 8 pointed out that the anlagen of the lungs and pancreas, which are derived from a common entodermal tube, are relatively close together and begin to appear almost simultaneously. They expressed the opinion that in the development of the pancreas and lungs, constriction of some of the excreting ducts and bronchial passages occurred. The resulting picture would resemble that seen in cases of experimentally produced obstruction in animals and in cases of fibrocystic disease of human beings. Oppenheimer 7 reported demonstration of obstruction of the duct of Wirsung in one case, she found only four other cases recorded in the literature. In our own cases serial histologic sections of the entire pancreas and of the head of the gland were studied in two cases, respectively, but no evidence of stenosis or atresia of the larger ducts could be demonstrated. However, this does "not rule out the possibility of obstruction in the smaller ducts and ductules. Some observers have pointed out that vitamin A deficiency may lead to obstruction of the pancreatic ducts by masses of desquamated epithelial cells. This was not observed in any of our cases and is probably a rare event. Most observers believe that vitamin A deficiency is probably not of primary etiologic importance but is a result or complication of fibrocystic disease. The almost constant occurrence of pulmonary suppuration and the histologic appearance of the pancreas have suggested that fibrocystic disease of the pancreas is due to infection, particularly those types caused by a filtrable virus. Brody 3 reported the finding of inclusion bodies in two of three cases of pancreatic fibrosis. Farber and Pratt 6, however, were unable to find inclusion bodies any more frequently on necropsy in cases of fibrocystic disease than in routine cases. No experimental evidence to support virus infection as a causative factor in fibrocystic disease of the pancreas has been reported. Blackfan and Wolbach 2, in 1933, and more recently Farber 5 advanced the thesis that fibrocystic disease is the result of abnormal pancreatic secretion. They -believed that an abnormally thick secretion caused intrinsic obstruction in the acini and small ducts. As a result, atrophy of acinar structures with condensation of the framework of connective tissue and growth of new fibrous tissue occurred. Farber also found inspissation of secretions and dilatation of ducts in the glands of the trachea, bronchi, esophagus, duodenum, gallbladder and intestinal tract. These changes, which were of the same general character as those in the pancreas, led to the conclusion that this disease is due to a generalized disorder that involves many glandular structures but exerts its greatest effect on the pancreas. Farber 4, moreover, produced the histologic picture of inspissation of secretion in the acini and small ducts of the pancreas of kittens by the administration of large doses of pilocarpine and mecholyl chloride (acetyl-/3-methylcholine chloride).
7 70 A. H. BAGGENSTOSS AND R. L. J. KENNEDY In our cases, the bronchi and their glands usually contained an exudate that was more purulent than mucoid but occasionally the bronchial glands were distended with mucous secretion. The only evidence of abnormal glandular secretion, except in these structures and the pancreas, was dilatation and distention of the glands of the duodenum. A number of explanations have been given for the development of pulmonary lesions. Decreased resistance as a result of malnutrition and vitamin deficiency is an obvious and no doubt logical explanation. Metaplasia of the bronchial epithelium as a result of vitamin A deficiency has been considered responsible for secondary infection. Obstruction of the bronchi by thick, tenacious mucous is doubtless an important predisposing factor and is probably responsible for early signs of atelectasis and emphysema, as well as later complications such as bronchiectasis and formation of abscesses. SUMMARY Fourteen cases of fibrocystic disease of the pancreas have been observed at necropsy at the Mayo Clinic over a period of eighteen years. These cases may be classified into three fairly distinct groups: In the first group (one case), the patient died of meconium ileus. In the second group (eight cases), the symptoms were predominantly respiratory in nature and the patients died of infection of the respiratory tract, usually during the first year of life. In the third group (five cases), the patients presented many symptoms of celiac disease. These patients also died of pulmonary infections, usually within a period of two years. Necropsy revealed varying amounts of pancreatic fibrosis and dilatation of the acini and ducts. Death, except in the case of the infant who died of meconium ileus, resulted from suppurative bronchitis, bronchiectasis and bronchopneumonia. The underlying cause of fibrocystic disease of the pancreas is unknown. Some observers have suggested that the condition is congenital in origin, resulting from obstruction of the pancreatic ducts. Although in some reported cases such obstruction has been demonstrated, this was not a finding in our cases. Other observers have suggested that the condition is attributable to vitamin A deficiency, infection and abnormal pancreatic secretion. The possibility that abnormally thick secretion causes intrinsic obstruction in the acini and small ducts must be seriously considered. REFERENCES (1) ANDERSEN, DOROTHY H.: Cystic fibrosis of the pancreas and its relation to celiac disease: a clinical and pathologic study. Am. J. Dis. Child., 56: 344, (2) BLACKFAN, K. D., AND WOLBACH, S. B.: Vitamin A deficiency in infants; a clinical and pathological study. J. Pediat., 3: 679, (3) BRODY, H.: Concerning the etiology of cystic fibrosis of the pancreas. (Abstr.) New York State J. Med., 41: 1256, (4) FARBER, SIDNEY: The experimental production of Achylia pancreatica. Am. J. Dis. Child., 64: 953, (5) FARBER, SIDNEY: Pancreatic insufficiency and the celiac syndrome. New England J. Med., 229: 653; 682, (6) FARBER, S., AND PRATT, EDWARD: Quoted by Farber, Sidney: Pancreatic function and disease in early life: V. Pathologic changes associated with pancreatic insufficiency in early life. Arch. Path., 36: 238, (7) OPPENHEIMER, ELLA H.: Congenital atresia of the pancreatic duct with cystic fibrosis of the pancreas. Arch. Path., 29: 790, (8) RAUCH, SOLOMON, LITVAK, A. M., AND STEINER, MATTHEW: Congenital familial steatorrhea with fibromatosis of pancreas and bronchiolectasis. J. Pediat., 14: 462, 1939.
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