Kaj Roholm Published his Seminal Study ‘Fluorine Intoxication’ in which He Described Three Phases of Bone Changes that Occur in skeletal Fluorosis

In 1937, Kaj Roholm published his seminal study Fluorine Intoxication in which he described three phases of bone changes that occur in skeletal fluorosis. (See below). These three phases, which are detectable by x-ray, have been widely used as a diagnostic guide for detecting the disease. They describe an osteosclerotic bone disease that develops first in the axial skeleton (the spine, pelvis, and ribs), and ultimately results in extensive calcification of ligaments and cartilage, as well as bony outgrowths such as osteophytes and exostoses.

Subsequent research has found, however, that x-rays provide a very crude measure for diagnosing fluorosis since the disease can cause symptoms and effects (e.g., osteoarthritis) before, and in the absence of, radiologicaly detectable osteosclerosis in the spine. Moreover, German scientists have expanded on Roholm’s description of the x-ray picture of the disease, by defining two additional phases (“subtle signs” & “stage O-I”) that occur prior to Roholm’s 3 phases. (See below). Research has found that individuals with these early skeletal phases can experience significant joint pain and stiffness. According to Franke (1975): “[W]e found patients with slight radiological changes (subtle signs or O-I) who complained of intense pains in the spine and in the large joints. On the other hand, some patients whose fluorosis was radiologically distinct were almost without complaints.”

Making matters even more complicated is the fact that numerous studies have found that fluorosis can cause a diverse range of skeletal changes beyond the predominantly osteosclerotic form of the disease that Roholm described. Strict reliance on Roholm’s description of classic fluorosis will thus frustrate efforts to detect, and prevent, skeletal fluoride poisoning.

Roholm (1937): The 3 Phases of Bone Changes in Skeletal fluorosis (Detectable by X-Ray):

“From the X-ray picture it is possible to differentiate between three phases of the same osteosclerotic process, each overlapping the next without any sharp boundary.

1st Phase.
“The changes are observed in pelvis and columna, but are doubtful or absent elsewhere. The density of bone is very little increased. The trabeculae are rough, blurred and give deep shadows; this is often distinct in corpora of the lower lumbar vertebrae. The bone has both a more prominent and a more blurred structure at the same time, which is very characteristic when the operator is familiar with the phenomenon, but otherwise is easily overlooked. The bone contour is sharp. In some few cases there is incipient osteophyte formation on the edge of corpora of the lumbar vertebrae. The boundary against the normal bone structure is not sharp, and in an isolated case it will be difficult to decide whether the change is a normal variation or a pathological finding. In serial examinations, however, the difference is distinct.

2nd Phase.

“The bone structure is blurred, the trabeculae merging together. Over often rather large areas the bone gives a diffuse, structureless shadow. At first glance the negative seems to have been underexposed, but it is difficult or impossible to distinguish details even when the time of exposure or the tension is increased. The bone contours are uneven and somewhat blurred. The changes are most distinct in pelvis and columna, but also in the ribs and in the bones of the extremities, even if there they are less pronounced and often resemble the changes described as 1st phase. In the extremity bones the medullary cavity is usually moderately narrowed. In columna there are incipient or moderate ligament calcifications, especially caudally; they appear in the form of pointed, beaked osteophytes with an inclination to form bridges between vertebral bodies or as a diffuse blur lying posteriorly to corpora. In some cases (particularly among the younger individuals) the ligament calcifications are absent, though the bone structure is so changed that the case must be placed to the 2nd phase.

3rd Phase. On the negative the bone presents itself as a more or less diffuse marble-white shadow, in which the details cannot be distinguished. Changes are observable in all bones but are still greatest centrally, being most conspicuous in bones with cancellous structure, pelvis, columna, ribs and sternum. In the bones of the extremities there are changes in the structure that recall the 2nd phase, or fairly often only the 1st phsase. Among the worst affected individuals changes are to be seen in the cranium, usually rather moderate in intensity. Theca is denser and gives a deeper shadow than normally, sutures and vessel grooves are indistinct, and the same applies to impressiones digitatae. The air-sinuses in the cranial bones are diminished in size. The region around sella turcica gives a deep shadow but is normal as to contour. No distinct thickening of the processus clinoidei was observed.

The bone contours almost everywhere are wooly and blurred. Very often the bones or certain parts of them have a rough and slightly enlarged appearance, but otherwise the shape is not altered. On the extremity bones are irregular periosteal thicknesses, some flats, others more rough. The interosseous membrane in antibrachium and crus are calcified to a greater or smaller extent. The normal cristae corresponding to the muscle attachments are increased in size and resemble exostoses. On costae, especially vertebrally, there is calcification of the insertions of the intercostal muscles, which appear like “rime frost needles” or irregular shadows to both sides. There are considerable ligament calcifications, varying up to very severe, in columna, particularly in pars lumbalis and thoracalis. In columna cervicalis these changes are less pronounced, but distinct. The ligament calcifications appear partly in the form of bridge-like connections with fairly sharp borders between corpora, partly as a diffuse opacity and density round about the intervertebral and costovertebral articulations. Processus transversi and spinosi are rough and thickened; between the latter are considerable ligament calcifications with irregular borders. In the pelvis, ligamentum sacrotuberosum is sometimes calcified. The intensity of the calcification and the diffuse density of the bone usually are in conformity with each other; in some elderly workers, however, there is a density of the osseous tissue which does not attain to the extreme degree, side by side with very pronounced ligament calcification.

In the extremity bones, both short and long, the medullary cavity is diminished in width and the boundary against compacta is less sharp than normally. The width of compacta is correspondingly increased. In tibia and femur the width of the medullary cavity sometimes decreases to half the normal, in metacarpals and phalanges there is sometimes a partial occlusion of the cavity.

The interarticular spaces are of normal width everywhere and the contours are sharp. Limited calcifications of the capsule in hip and knee joints are seen. The intervertebral disks are not visibly changed and the calcification of the costal cartilage does not exceed the normal.

If the result of the Rontgen examination is to be summarized, the first thing to emphasize is the fact that the affection is a system-disease, for it attacks all bones, though it has a predilection for certain places. The pathological process may be characterized as a diffuse osteosclerosis, in which the pathological formation of bone starts both in periosteum and in endosteum. Compacta densifies and thickens; the spongiosa trabecula thicken and fuse together. The medullary cavity decreases in diameter. There is a considerable new-formation of bone from periosteum, and ligaments that normally do not calcify or only in advanced age undergo a considerable degree of calcification. All signs of bone destruction are absent from the picture.”

SOURCE: Roholm K. (1937). Fluoride intoxication: a clinical-hygienic study with a review of the literature and some experimental investigations. London: H.K. Lewis Ltd. pp. 141-143


Below are selected quotes from Danish researcher Kaj Roholm’s 1937 book Fluorine Intoxication. All emphasis is original. Roholm reviewed the state of knowledge regarding acute and chronic fluorine poisoning at that time, and also described his own investigation into cryolite factory workers in Copenhagen, and his experiments on animals. Note that “fluorine” here refers predominantly to various forms of fluoride, including cryolite, not fluorine gas, though some covalent fluorine compounds are mentioned. Fluoride is the ionic form of fluorine.

It has to be said that although the bone and ligament changes in cryolite workers observed by Roholm are certainly of interest, as far as providing a representative sample of the general population of working age is concerned, the workers at the Copenhagen cryolite factory were about as bad as it gets. Evidently a large proportion of those who started work there could not tolerate the working conditions for long, which is likely to have been due to the fluoride poisoning they were suffering in most cases. Therefore most or all of those who were unusually susceptible to fluoride toxicity would have been weeded out, and probably also many with approximately average susceptibility. Effects on joint function were inherently self-limiting, because if a worker’s ability to do the job was seriously impaired they would presumably no longer be employed at the factory, and hence be removed from the source of high fluoride exposure. Also, the youngest worker was 20 years of age. Some of the workers may have started at an earlier age, but there is no reason to believe that any were exposed to fluoride at the factory throughout their lives, or as foetuses, in contrast to the situation with forced-fluoridation. Roholm’s investigation also lacked a control group and was not longitudinal, and must therefore be regarded as revealing only the tip of the chronic fluoride poisoning iceberg.

To mention a few highlights from other parts of the book, Roholm’s comparison of the abundance in the earth’s crust of fluorine with that of lead, arsenic and mercury has a touch of the prophetic about it, considering that all four are now known to be developmental neurotoxicants, and not nutrients. He confirms that sodium fluoride and sodium fluosilicate were used as mouse and rat poison. He is also adamant that fluoride is not necessary for healthy teeth. More than 75 years later, the US Institute of Medicine and others are still trying to claim that fluoride is some kind of quasi-nutrient.

p 2 “In commerce we find hydrofluoric acid and hydrofluosilicic acid, the minerals fluorspar (CaF2) and cryolite (Na3AlF6), silicofluorides, which are a by-product of superphosphate manufacturing, and divers synthetically made fluorides.”

p 3 “Fluorine minerals have been known since the Middle Ages.”

p 4 “A dental disease in man, mottled enamel, which Black and McKay described in 1916 as occurring in Colorado, has proved to be rather widely distributed in several parts of the world. The aetiology was unknown until 1931, when Smith, Lantz and Smith demonstrated by means of animal experiments that the disease was caused by a relatively high fluorine content in the drinking water. Independently of their work, Velu proved that a common dental ailment in North Africa among animals and man, darmous, was of the same origin.

Since the close of last century there are records of a number of cases of acute poisoning in man by various fluorine compounds. Chronic human poisoning with bone symptoms was described for the first time in 1932, by Flemming, Moller and Gudjonsson, in cryolite workers.”

p 9 “In practice it is assumed that highly diluted solutions of hydrofluoric acid are not dangerous; this, however, to a great extent depends upon how long the influence is allowed to act.”

p 26 “In Table 4 I have summarized the various symptoms in 34 cases of fatal poisoning. Broadly speaking the symptoms may be gathered into two groups, one expressing an acute local irritation of the gastro-intestinal canal, the other indicating both an irritating and a paralysing effect on the central nervous system or musculature.” This indicates neurotoxicity.

p 33 “Caries does not seem to be especially frequent in the moderately attacked [by dental fluorosis] teeth. Still, the enamel is more brittle than normally, is inclined to chip off, and fillings do not hold well.”

p 33 “At the time of Black and McKay’s investigations [into mottled enamel] it was the popular belief that the anomaly was associated with drinking water, especially from artesian wells. Where the water supply was changed it was possible to stop the development of the anomaly in an affected region. Analyses of the water showed nothing abnormal, however.”

p 34 “We may now regard it as an established fact that mottled enamel is caused by a relatively high fluorine content in drinking water.”

p 46 “According to Washington, who embarked on a calculation of the chemical composition of the earth’s crust, fluorine stands thirteenth among the elements in order of importance, before the other halogens and far ahead of toxic elements like lead, arsenic and mercury. Phosphorus occupies the tenth place with 0.13 per cent.; fluorine is at 0.077 per cent.”

p 46 “Of particular importance is the rich occurrence of native phosphate or phosphorite, deposits of calcium phosphate in amorphous form, the raw material in the manufacture of superphosphate. In almost every case they contain fluorine, most frequently 2 to 5 per cent., varying in the different deposits.”

p 53 “In 1803 Morichini observed the evolution of hydrofluoric acid vapours when treating a fossil elephant tooth with sulphuric acid.”

p 60 “Isolated cells or tissue placed in a solution of sodium fluoride are destroyed quickly as compared with equimolecular solutions of the sodium salts of the other halogens. In this respect fluorine stands out from the group.”

p 70 “The apparent difference in the toxicity of sodium fluoride and sodium fluosilicate lies in the different fluorine content. (NaF: 45.24 per cent. F; Na2SiF6: 60.54 per cent. F). Allowance being made for this, the two compounds are equally toxic, even with parenteral administration.”

p 84 “A series of rat experiments at Iowa Agricultural Experimental Station showed that on a diet containing fluorine the succeeding generations were less prolific than the first generation”

p 93 “Fluorine has a detrimental effect on the growth of the teeth, whereby the part of a tooth calcifying during the period fluorine intake will acquire permanent defects.”

p 104 “As a rule the excreted quantity [of fluoride] was about half of the intake [in a dog].”

p 106 “Fluorine seems mostly to be excreted in the urine, in what form is not known.”

p 112 “Bones were skeletonized very carefully, and periosteum and marrow removed as far as possible. Soxhlet’s apparatus, or a rotating benzine drum, was used for defatting. The material abstract it for analysis was carbonized at low temperature and pulverized in an iron mortar. Incineration proceeded as with the organs, as a rule taking 3-5 hours. No calcium oxyde was added to bones and teeth. [details of Roholm’s investigation]”

p 130 “The pay [at the cryolite factory] is relatively good, partly based on piece-work. The working week consists of 48 hours. For a number of years the workers have had a week’s summer holiday with pay, and with every form of illness about one-fourth of the wage in sick benefit for a maximum of 13 weeks. On discharge, older, deserving workers receive a small pension. The drawbacks are, apart from the toxic effect of the cryolite, the generally laborious character of the work and the almost omnipresent dust.”

p 131/2 “During the past ten years for which it has been possible to obtain information, a certain number of the workers have only been employed a short time; it is possible that to a certain degree this is due to the character of the work. In the period comprised by Table 19, 23 men (16.2 per cent.) and 39 women (19.6 per cent.) worked for less than a month. In both groups are persons who were only one or few days at work and have not since been taken on again. It seems probable that for these workers it may just as well have been discomfort at the work as unfitness for it. No doubt the work makes considerable demands on the physique, but otherwise it is not especially exacting for the great majority of the workers. The relatively large number of re-engagements in both the male and the female group (16.9 and 26.8 per cent.) on the other hand indicates that the drawbacks of the work are not deterringly great. Similar importance may be attached to the circumstance that many of the former and present workers are related to one another. Though most of the workers in the period have worked for less than two years, a number have been employed for much longer: sixteen, of both sexes (4.7 per cent.) for ten years or more, generally uninterruptedly. As will be seen later, the average period of employment for the persons working at the time of this investigation was much longer (10 years). Although suitable comparative material is lacking, it would seem to appear from the statistics, however, that the work is connected with certain drawbacks, the effect of which is that the average period of employment is rather short, but that the injurious effect is not so considerable that it prevents employment over a long stretch of years.”

p 132 “No worker was under 20 years of age.”

p 132 “In many cases the length of employment was considerable, on an average 10 years; 21 workers (30.9 per cent.) had worked there for ten years or more, 5 workers (7.4 per cent.) for 25 years or more. This picture of the length of employment is much more favourable than that of conditions considered over a longer period of years (Table 19). Probably the cause of this is that the number of hands at the factory has gone down in the course of the last few years and that on principle the hands of the discharged were those who had been employed the shortest time. Still, there is no doubt that some selection is made, whereby workers who tolerate the work best remain longest at the factory.”

p 134 “With the assistance of the factory’s books a search was also made for former workers, and it was possible to get in touch with 131 people, 69 men and 62 women, who had worked at the factory for at least six months.”

p 136/7 “Symptoms to be recorded had to be of a certain intensity or duration, so that accidental feelings and the like were disregarded. Naturally a certain amount of error is inherent in personal decisions of this kind. In such a method the numerical statement of symptom frequency leaves a summary, massive impression that does not correspond to the discomforts present at the daily work. Only two of the workers, one male and one female, denied ever having felt discomfort from the work or having noticed morbid symptoms at all. The others indicated a whole conglomeration of symptoms which are recorded in Table 22 according to frequency. The commonest complaints were of various dyspeptic phenomena, shortness of breath and rheumatic attacks.”

p 138 “The rule is that for a period of some few days to some few weeks after starting at the factory worker suffers from these acute gastric attacks, whereafter they disappear, especially the nausea and vomiting. Thereafter some of the workers tolerate the dust without observing the symptoms; others will still have transitory symptoms after holidays, or if the dust quantity temporarily becomes especially high.”

p 141 “The bone changes are very characteristic and form the basis for a division of the disease into phases.”

p 141-6 “1st Phase.

The changes are observed in pelvis and columna, but are doubtful or absent elsewhere. The density of the bone is very little increased. The trabeculae are rough, blurred and give deep shadows; this is often distinct in corpora of the lower lumbar vertebrae. The bone has both a more prominent and a more blurred structure at the same time, which is very characteristic when the operator is familiar with the phenomenon, but otherwise is easily overlooked (Fig. 17). The bone contour is sharp. In some few cases there is incipient osteophyte formation on the edge of corpora of the lumbar vertebrae. The boundary against the normal bone structure is not sharp, and in an isolated case it will be difficult to decide whether the change is a normal variation or a pathological finding. In serial examinations, however, the difference is distinct.

2nd Phase.

The bone structure is blurred, the trabeculae merging together. Over often rather large areas the bone gives a diffuse, structureless shadow. At first glance the negative seems to have been underexposed, but it is difficult or impossible to distinguish details even when the time of exposure or the tension is increased. The bone contours are uneven and somewhat blurred. The changes are most distinct in pelvis (Fig. 18) and columna (Fig. 20), but also in the ribs (Fig. 27) and in the bones of the extremities, even if there they are less pronounced and often resemble the changes described as 1st phase. In the extremity bones the medullary cavity is usually moderately narrowed. In columna there are incipient or moderate ligament calcifications, especially caudally; they appear in the form of pointed, beaked osteophytes with an inclination to form bridges between the vertebral bodies or as a diffuse blur lying posteriorly to corpora. In some cases (particularly among the younger individuals) the ligament calcifications are absent, though the bone structure is so changed that the case must be placed to be 2nd phase.

Continued on next page…

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