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Scurvy

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Scurvy
Other namesMoeller's disease, Cheadle's disease, scorbutus,[1] Barlow's disease, hypoascobemia[1]
Scorbutic gums, a symptom of scurvy. Note gingival redness in the triangle-shaped area between the teeth
SpecialtyEndocrinology
SymptomsWeakness, feeling tired, changes to hair, sore arms and legs, gum disease, easy bleeding[1][2]
CausesNot enough vitamin C[1]
Risk factorsMental disorders, unusual eating habits, alcoholism, old people who live alone, intestinal malabsorption, dialysis[2]
Diagnostic methodBased on symptoms[2]
TreatmentVitamin C supplements[1]
FrequencyRare[2]

Scurvy is a disease resulting from a lack of vitamin C.[1] Early symptoms include weakness, feeling tired, and sore arms and legs.[1][2] Without treatment, decreased red blood cells, gum disease, changes to hair, and bleeding from the skin may occur.[1][3] As scurvy worsens there can be poor wound healing, personality changes, and finally death from infection or bleeding.[2]

Typically, scurvy is caused by a lack of vitamin C in the diet.[1] It takes at least a month of little to no vitamin C before symptoms occur.[1][2] In modern times, it occurs most commonly in people with mental disorders, unusual eating habits, alcoholism, and old people who live alone.[2] Other risk factors include intestinal malabsorption and dialysis.[2] Humans and certain other animals require vitamin C in their diets to make the building blocks for collagen.[2] Diagnosis typically is based on physical signs, X-rays, and improvement after treatment.[2]

Treatment is with vitamin C supplements taken by mouth.[1] Improvement often begins in a few days with complete recovery in a few weeks.[2] Sources of vitamin C in the diet include citrus fruit and a number of vegetables such as tomatoes and potatoes.[2] Cooking often decreases vitamin C in foods.[2]

Scurvy currently is rare.[2] It occurs more often in the developing world in association with malnutrition.[2] Rates among refugees are reported at 5% to 45%.[4] Scurvy was described as early as the time of ancient Egypt.[2] It was a limiting factor in long distance sea travel, often killing large numbers of people.[5] A Scottish surgeon in the Royal Navy, James Lind, was the first to prove it could be treated with citrus fruit in a 1753 publication.[2][6] His experiments represented the first controlled trial. It took another 40 years before the British Navy began giving out lemon juice routinely.[7]

Signs and symptoms

Early symptoms are malaise and lethargy. Even earlier might be a pain in a section of the gums which interferes with digestion. After 1–3 months, patients develop shortness of breath and bone pain. Myalgias may occur because of reduced carnitine production. Other symptoms include skin changes with roughness, easy bruising and petechiae, gum disease, loosening of teeth, poor wound healing, and emotional changes (which may appear before any physical changes). Dry mouth and dry eyes similar to Sjögren's syndrome may occur. In the late stages, jaundice, generalized edema, oliguria, neuropathy, fever, convulsions, and eventual death are frequently seen.[8]

  • A child presenting a "scorbutic tongue" due to what proved to be a vitamin C deficiency.
    A child presenting a "scorbutic tongue" due to what proved to be a vitamin C deficiency.
  • A child with scurvy in flexion posture.
    A child with scurvy in flexion posture.
  • Photo of the chest cage with pectus excavatum and scorbutic rosaries.
    Photo of the chest cage with pectus excavatum and scorbutic rosaries.

Cause

Scurvy or subclinical scurvy is caused by a deficiency of vitamin C. In modern Western societies, scurvy is rarely present in adults, although infants and elderly people are affected.[9] Virtually all commercially available baby formulas contain added vitamin C. Human breast milk contains sufficient vitamin C, if the mother has an adequate intake. Commercial milk is pasteurized, a heating process that destroys the natural vitamin C content of the milk.

Scurvy is one of the accompanying diseases of malnutrition (other such micronutrient deficiencies are beriberi or pellagra) and thus is still widespread in areas of the world depending on external food aid.[10] Although rare, there are also documented cases of scurvy due to poor dietary choices by people living in industrialized nations.[11][12][13][14][15]

Pathogenesis

X-ray of the knee joint (arrow indicates scurvy line).

Ascorbic acid is needed for a variety of biosynthetic pathways, by accelerating hydroxylation and amidation reactions. In the synthesis of collagen, ascorbic acid is required as a cofactor for prolyl hydroxylase and lysyl hydroxylase. These two enzymes are responsible for the hydroxylation of the proline and lysine amino acids in collagen. Hydroxyproline and hydroxylysine are important for stabilizing collagen by cross-linking the propeptides in collagen. Defective collagen fibrillogenesis impairs wound healing. Collagen is an important part of bone, so bone formation is affected. Defective connective tissue leads to fragile capillaries, resulting in abnormal bleeding. Untreated scurvy is invariably fatal.[16]

Prevention

Scurvy can be prevented by a diet that includes vitamin C-rich foods such as bell peppers (sweet peppers), blackcurrants, broccoli, chile peppers, guava, kiwifruit, and parsley. Other sources rich in vitamin C are fruits such as lemons, oranges, papaya, and strawberries. It is also found in vegetables, such as brussels sprouts, cabbage, potatoes, and spinach. Some fruits and vegetables not high in vitamin C may be pickled in lemon juice, which is high in vitamin C. Though redundant in the presence of a balanced diet,[17] various nutritional supplements are available that provide ascorbic acid well in excess of that required to prevent scurvy.

Some animal products, including liver, Muktuk (whale skin), oysters, and parts of the central nervous system, including the adrenal medulla, brain, and spinal cord, contain large amounts of vitamin C, and can even be used to treat scurvy. Fresh meat from animals which make their own vitamin C (which most animals do) contains enough vitamin C to prevent scurvy, and even partly treat it. In some cases (notably French soldiers eating fresh horse meat), it was discovered that meat alone, even partly cooked meat, could alleviate scurvy. Conversely, in other cases, a meat-only diet could cause scurvy.[18]

Scott's 1902 Antarctic expedition used lightly fried seal meat and liver, whereby complete recovery from incipient scurvy was reported to have taken less than two weeks.[19]

History

Hippocrates documented scurvy as a disease,[20][21] and Egyptians have recorded its symptoms as early as 1550 BCE.[22] The knowledge that consuming foods containing vitamin C is a cure for scurvy has been repeatedly rediscovered and forgotten into the early 20th century.[23]

Early modern era

In the 13th century, the Crusaders frequently suffered from scurvy. In the 1497 expedition of Vasco de Gama, the curative effects of citrus fruit were already known[23][24] and confirmed by Pedro Álvares Cabral and his crew in 1507.[25]

The Portuguese planted fruit trees and vegetables in Saint Helena, a stopping point for homebound voyages from Asia, and left their sick, suffering from scurvy and other ailments, to be taken home, if they recovered, by the next ship.[26]

In 1500, one of the pilots of Cabral's fleet bound for India noted that in Malindi, its king offered the expedition fresh supplies such as lambs, chickens, and ducks, along with lemons and oranges, due to which "some of our ill were cured of scurvy".[27][28]

Unfortunately, these travel accounts have not stopped further maritime tragedies caused by scurvy, first because of the lack of communication between travelers and those responsible for their health, and because fruits and vegetables could not be kept for long on ships.[29]

In 1536, the French explorer Jacques Cartier, exploring the St. Lawrence River, used the local natives' knowledge to save his men who were dying of scurvy. He boiled the needles of the arbor vitae tree (Eastern White Cedar) to make a tea that was later shown to contain 50 mg of vitamin C per 100 grams.[30][31] Such treatments were not available aboard ship, where the disease was most common. In February 1601, Captain James Lancaster, while sailing to Sumatra, landed on the northern coast to specifically obtain lemons and oranges for his crew to stop scurvy.[32] During the Age of Exploration (between 1500 and 1800), it has been estimated that scurvy killed at least two million sailors.[33] Jonathan Lamb wrote: "In 1499, Vasco da Gama lost 116 of his crew of 170; In 1520, Magellan lost 208 out of 230;...all mainly to scurvy."[34]

In 1593, Admiral Sir Richard Hawkins advocated drinking orange and lemon juice as a means of preventing scurvy.[35]

In 1614, John Woodall, Surgeon General of the East India Company, published "The Surgion's Mate" as a handbook for apprentice surgeons aboard the company's ships. He repeated the experience of mariners that the cure for scurvy was fresh food or, if not available, oranges, lemons, limes, and tamarinds.[36] He was, however, unable to explain the reason why, and his assertion had no impact on the opinions of the influential physicians who ran the medical establishment that scurvy was a digestive complaint.

18th century

James Lind, a pioneer in the field of scurvy prevention

A 1707 handwritten book by Mrs. Ebot Mitchell, discovered in a house in Hasfield, Gloucestershire, contains a "Recp.t for the Scurvy" that consisted of extracts from various plants mixed with a plentiful supply of orange juice, white wine or beer.[37]

In 1734, the Leiden-based physician Johann Bachstrom published a book on scurvy in which he stated, "scurvy is solely owing to a total abstinence from fresh vegetable food, and greens; which is alone the primary cause of the disease", and urged the use of fresh fruit and vegetables as a cure.[38][39][40]

However, it was not until 1747 that James Lind formally demonstrated that scurvy could be treated by supplementing the diet with citrus fruit, in the first ever clinical trial.[6] In 1753, Lind published A Treatise of the Scurvy, in which he explained the details of his clinical trial, but it occupied only a few paragraphs in a work that was long and complex and had little impact. In fact, Lind himself never actively promoted lemon juice as a single ‘cure’. He shared medical opinion at the time that scurvy had multiple causes – notably hard work, bad water, and the consumption of salt meat in a damp atmosphere which inhibited healthful perspiration and normal excretion - and therefore required multiple solutions.[41] He was also sidetracked by the possibilities of producing a concentrated ‘rob’ of lemon juice by boiling it. Unfortunately this process destroyed the vitamin C and was unsuccessful.

During the 18th century, disease killed more British sailors than enemy action. It was mainly by scurvy that George Anson, in his celebrated voyage of 1740–1744, lost nearly two-thirds of his crew (1300 out of 2000) within the first 10 months of the voyage.[42] The Royal Navy enlisted 184,899 sailors during the Seven Years' War; 133,708 of these were "missing" or died from disease, and scurvy was the leading cause.[43]

Although throughout this period sailors and naval surgeons were increasingly convinced that citrus fruits could cure scurvy, the classically trained physicians who ran the medical establishment dismissed this evidence as mere anecdote which did not conform to current theories of disease. Literature championing the cause of citrus juice, therefore, had no practical impact. Medical theory was based on the assumption that scurvy was a disease of internal putrefaction brought on by faulty digestion caused by the hardships of life at sea and the naval diet. Although this basic idea was given different emphases by successive theorists, the remedies they advocated (and which the navy accepted) amounted to little more than the consumption of ‘fizzy drinks’ to activate the digestive system, the most extreme of which was the regular consumption of ‘elixir of vitriol’ – sulphuric acid taken with spirits and barley water, and laced with spices.

In 1764, a new variant appeared. Advocated by Dr David McBride and Sir John Pringle, Surgeon General of the Army and later President of the Royal Society, this idea was that scurvy was the result of a lack of ‘fixed air’ in the tissues which could be prevented by drinking infusions of malt and wort whose fermentation within the body would stimulate digestion and restore the missing gases.[44] These ideas received wide and influential backing, when James Cook set off to circumnavigate the world (1768–1771) in HM Bark Endeavour, malt and wort were top of the list of the remedies he was ordered to investigate. The others were beer, sour crout and Lind's ‘rob’. The list did not include lemons.[45]

Cook did not lose a single man to scurvy, and his report came down in favour of malt and wort, although it is now clear that the reason for the health of his crews on this and other voyages was Cook's regime of shipboard cleanliness, enforced by strict discipline, as well as frequent replenishment of fresh food and green stuffs.[46] Another rule implemented by Cook was his prohibition of the consumption of salt fat skimmed from the ship's copper boiling pans, then a common practice in the Navy. In contact with air the copper formed compounds that prevented the absorption of vitamins by the intestines.[47]

The first major long distance expedition that experienced virtually no scurvy was that of the Spanish naval officer Alessandro Malaspina, 1789–1794. Malaspina's medical officer, Pedro González, was convinced that fresh oranges and lemons were essential for preventing scurvy. Only one outbreak occurred, during a 56-day trip across the open sea. Five sailors came down with symptoms, one seriously. After three days at Guam all five were healthy again. Spain's large empire and many ports of call made it easier to acquire fresh fruit.[48]

Although towards the end of the century MacBride's theories were being challenged, the medical establishment in Britain remained wedded to the notion that scurvy was a disease of internal ‘putrefaction’ and the Sick and Hurt Board, run by administrators, felt obliged to follow its advice. Within the Royal Navy, however, opinion – strengthened by first-hand experience of the use of lemon juice at the siege of Gibraltar and during Admiral Rodney's expedition to the Caribbean – had become increasingly convinced of its efficacy. This was reinforced by the writings of experts like Gilbert Blane[49] and Thomas Trotter[50] and by the reports of up-and-coming naval commanders.

With the coming of war in 1793, the need to eliminate scurvy acquired a new urgency. But the first initiative came not from the medical establishment but from the admirals. Ordered to lead an expedition against Mauritius, Rear Admiral Gardner was uninterested in the wort, malt and elixir of vitriol which were still being issued to ships of the Royal Navy, and demanded that he be supplied with lemons, to counteract scurvy on the voyage. Members of the Sick and Hurt Board, recently augmented by two practical naval surgeons, supported the request, and the Admiralty ordered that it be done. There was, however, a last minute change of plan. The expedition against Mauritius was cancelled. On 2 May 1794, only HMS Suffolk and two sloops under Commodore Peter Rainier sailed for the east with an outward bound convoy, but the warships were fully supplied with lemon juice and the sugar with which it had to be mixed. Then in March 1795, came astonishing news. Suffolk had arrived in India after a four-month voyage without a trace of scurvy and with a crew that was healthier than when it set out.

The effect was immediate. Fleet commanders clamoured also to be supplied with lemon juice, and by June the Admiralty acknowledged the groundswell of demand in the navy had agreed to a proposal from the Sick and Hurt Board that lemon juice and sugar should in future be issued as a daily ration to the crews of all warships.[51]

It took a few years before the method of distribution to all ships in the fleet had been perfected and the supply of the huge quantities of lemon juice required to be secured, but by 1800, the system was in place and functioning. This led to a remarkable health improvement among the sailors and consequently played a critical role in gaining the advantage in naval battles against enemies who had yet to introduce the measures.

19th century

Page from the journal of Henry Walsh Mahon showing the effects of scurvy, from his time aboard HM Convict Ship Barrosa (1841/2)

The surgeon-in-chief of Napoleon's army at the Siege of Alexandria (1801), Baron Dominique-Jean Larrey, wrote in his memoirs that the consumption of horse meat helped the French to curb an epidemic of scurvy. The meat was cooked but was freshly obtained from young horses bought from Arabs, and was nevertheless effective. This helped to start the 19th-century tradition of horse meat consumption in France.[52]

Lauchlin Rose patented a method used to preserve citrus juice without alcohol in 1867, creating a concentrated drink known as Rose's lime juice. The Merchant Shipping Act of 1867 required all ships of the Royal Navy and Merchant Navy to provide a daily lime ration to sailors to prevent scurvy.[citation needed] The product became nearly ubiquitous, hence the term "limey", first for British sailors, then for English immigrants within the former British colonies (particularly America, New Zealand and South Africa), and finally, in old American slang, all British people.[53]

The plant Cochlearia officinalis, also known as "Common Scurvygrass", acquired its common name from the observation that it cured scurvy, and it was taken on board ships in dried bundles or distilled extracts. Its very bitter taste was usually disguised with herbs and spices; however, this did not prevent scurvygrass drinks and sandwiches from becoming a popular fad in the UK until the middle of the nineteenth century, when citrus fruits became more readily available.[54]

West Indian limes began to supplement lemons, when Spain's alliance with France against Britain in the Napoleonic Wars made the supply of Mediterranean lemons problematic, and because they were more easily obtained from Britain's Caribbean colonies[23] and were believed to be more effective because they were more acidic. It was the acid, not the (then-unknown) Vitamin C that was believed to cure scurvy. In fact, the West Indian limes were significantly lower in Vitamin C than the previous lemons and further were not served fresh but rather as lime juice, which had been exposed to light and air, and piped through copper tubing, all of which significantly reduced the Vitamin C. Indeed, a 1918 animal experiment using representative samples of the Navy and Merchant Marine's lime juice showed that it had virtually no antiscorbutic power at all.[23]

The belief that scurvy was fundamentally a nutritional deficiency, best treated by consumption of fresh food, particularly fresh citrus or fresh meat, was not universal in the 19th and early 20th centuries, and thus sailors and explorers continued to suffer from scurvy into the 20th century. For example, the Belgian Antarctic Expedition of 1897–1899 became seriously affected by scurvy when its leader, Adrien de Gerlache, initially discouraged his men from eating penguin and seal meat.

In the Royal Navy's Arctic expeditions in the 19th century it was widely believed that scurvy was prevented by good hygiene on board ship, regular exercise, and maintaining the morale of the crew, rather than by a diet of fresh food. Navy expeditions continued to be plagued by scurvy even while fresh (not jerked or tinned) meat was well known as a practical antiscorbutic among civilian whalers and explorers in the Arctic. Even cooking fresh meat did not entirely destroy its antiscorbutic properties, especially as many cooking methods failed to bring all the meat to high temperature.

The confusion is attributed to a number of factors:[23]

  • while fresh citrus (particularly lemons) cured scurvy, lime juice that had been exposed to light, air and copper tubing did not – thus undermining the theory that citrus cured scurvy;
  • fresh meat (especially organ meat and raw meat, consumed in arctic exploration) also cured scurvy, undermining the theory that fresh vegetable matter was essential to preventing and curing scurvy;
  • increased marine speed via steam shipping, and improved nutrition on land, reduced the incidence of scurvy – and thus the ineffectiveness of copper-piped lime juice compared to fresh lemons was not immediately revealed.

In the resulting confusion, a new hypothesis was proposed, following the new germ theory of disease – that scurvy was caused by ptomaine, a waste product of bacteria, particularly in tainted tinned meat.

Infantile scurvy emerged in the late 19th century because children were being fed pasteurized cow's milk, particularly in the urban upper class. While pasteurization killed bacteria, it also destroyed vitamin C. This was eventually resolved by supplementing with onion juice or cooked potatoes.

20th century

By the early 20th century, when Robert Falcon Scott made his first expedition to the Antarctic (1901–1904), the prevailing theory was that scurvy was caused by "ptomaine poisoning", particularly in tinned meat.[55] However, Scott discovered that a diet of fresh meat from Antarctic seals cured scurvy before any fatalities occurred.[56]

In 1907, an animal model which would eventually help to isolate and identify the "antiscorbutic factor" was discovered. Axel Holst and Theodor Frølich, two Norwegian physicians studying shipboard beriberi contracted by ship's crews in the Norwegian Fishing Fleet, wanted a small test mammal to substitute for the pigeons then used in beriberi research. They fed guinea pigs their test diet of grains and flour, which had earlier produced beriberi in their pigeons, and were surprised when classic scurvy resulted instead. This was a serendipitous choice of animal. Until that time, scurvy had not been observed in any organism apart from humans and had been considered an exclusively human disease. (Some birds are susceptible to scurvy, but pigeons are unaffected by scurvy, as they produce vitamin C.) Holst and Frølich found they could cure scurvy in guinea pigs with the addition of various fresh foods and extracts. This discovery of an animal experimental model for scurvy, which was made even before the essential idea of "vitamins" in foods had been put forward, has been called the single most important piece of vitamin C research.[57]

Vilhjalmur Stefansson, an arctic explorer who had lived among the Inuit, proved that the all-meat diet they consumed did not lead to vitamin deficiencies. He participated in a study in New York's Bellevue Hospital in February 1928, where he and a companion ate only meat for a year while under close medical observation, yet remained in good health.[58]

In 1927, Hungarian biochemist Szent-Györgyi isolated a compound he called "hexuronic acid".[59] Szent-Györgyi suspected hexuronic acid, which he had isolated from adrenal glands, to be the antiscorbutic agent, but he could not prove it without an animal-deficiency model. In 1932, the connection between hexuronic acid and scurvy was finally proven by American researcher Charles Glen King of the University of Pittsburgh.[60] King's laboratory was given some hexuronic acid by Szent-Györgyi and soon established that it was the sought-after anti-scorbutic agent. Because of this, hexuronic acid was subsequently renamed ascorbic acid.

21st century

In the 2010s, scurvy hasn't entirely disappeared from developed countries. Rates of incidence, while still very low, are increasing in the United Kingdom according to NHS Digital.[61] Several cases were also reported in Westmead Hospital, Sydney, Australia.[62]

Human trials

Notable human dietary studies of experimentally induced scurvy have been conducted on conscientious objectors during WWII in Britain and on Iowa state prisoner volunteers in the late 1960s. These studies both found that all obvious symptoms of scurvy previously induced by an experimental scorbutic diet with extremely low vitamin C content could be completely reversed by additional vitamin C supplementation of only 10 mg per day. In these experiments, no clinical difference was noted between men given 70 mg vitamin C per day (which produced blood levels of vitamin C of about 0.55 mg/dl, about 1/3 of tissue saturation levels), and those given 10 mg per day (which produced lower blood levels). Men in the prison study developed the first signs of scurvy about 4 weeks after starting the vitamin C-free diet, whereas in the British study, six to eight months were required, possibly because the subjects were pre-loaded with a 70 mg/day supplement for six weeks before the scorbutic diet was fed.[63]

Men in both studies, on a diet devoid or nearly devoid of vitamin C, had blood levels of vitamin C too low to be accurately measured when they developed signs of scurvy, and in the Iowa study, at this time were estimated (by labeled vitamin C dilution) to have a body pool of less than 300 mg, with daily turnover of only 2.5 mg/day.[64]

Other animals

Scurvy does not occur in most animals as they can make their own vitamin C. However, humans and other higher primates (the simians—monkeys and apes—and tarsiers), guinea pigs, most or all bats, and some species of birds and fish lack an enzyme (L-gulonolactone oxidase) necessary for such synthesis and must obtain vitamin C through their diet. The gene for L-gulonolactone oxidase is still present in the human genome, but deactivated by DNA mutations.

Almost all plant and animal species synthesize vitamin C. Notable mammalian exceptions include most or all of the order Chiroptera (bats), and one of the two major primate suborders, the "Anthropoidea" (Haplorrhini) which include tarsiers, monkeys, and apes, including human beings. The Strepsirrhini (non-tarsier prosimians) can make their own vitamin C, and these include lemurs, lorises, pottos, and galagos. Ascorbic acid is also not synthesized by at least two species of Caviidae, the capybara[65] and the guinea pig. There are known species of birds and fish that do not synthesize their own Vitamin C. All species that do not synthesize ascorbate require it in the diet. Deficiency causes scurvy in humans, and somewhat similar symptoms in other animals.[66][67][68]

Name

In babies, scurvy is sometimes referred to as Barlow's disease, named after Thomas Barlow,[69] a British physician who described it in 1883.[70] However, Barlow's disease may also refer to mitral valve prolapse.

References

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  24. ^ As they sailed farther up the east coast of Africa, they met local traders, who traded them fresh oranges. Within 6 days of eating the oranges, da Gama's crew recovered fully and he noted, "It pleased God in his mercy that … all our sick recovered their health for the air of the place is very good." Infantile Scurvy: A Historical Perspective, Kumaravel Rajakumar, MD
  25. ^ "Relação do Piloto Anônimo", narrativa publicada em 1507 sobre a viagem de Pedro Álvares Cabral às Índias, indicava que os "refrescos" oferecidos aos portugueses pelo rei de Melinde eram o remédio eficaz contra a doença (Nava, 2004). A medicina nas caravelas - Século XV, Cristina B. F. M. Gurgel I; Rachel Lewinsohn II, Marujos, Alimentação e Higiene a Bordo
  26. ^ On returning, Lopes' ship had left him on St Helena, where with admirable sagacity and industry he planted vegetables and nurseries with which passing ships were marvellously sustained. [...] There were 'wild groves' of oranges, lemons and other fruits that ripened all the year round, large pomegranates and figs. Santa Helena, A Forgotten Portuguese Discovery, Harold Livermore – Estudos em Homenagem a Luis Antonio de Oliveira Ramos, Faculdade de Letras da Universidade do Porto, 2004, p. 630-631
  27. ^ Logo que chegámos mandou-nos El Rey visitar e ao mesmo tempo um refresco de carneiros, galinhas, patos, limões e laranjas, as melhores que há no mundo, e com ellas sararam de escorbuto alguns doentes que tinhamos connosco in Portuguese, in Pedro Álvares Cabral, Metzer Leone Editorial Aster, Lisbon, p.244
  28. ^ Germano de Sousa (2013) História da Medicina Portuguesa Durante a Expansão, Círculo de Leitores, Lisbon, p.129
  29. ^ Contudo, tais narrativas não impediram que novas tragédias causadas pelo escorbuto assolassem os navegantes, seja pela falta de comunicação entre os viajantes e responsáveis pela sua saúde, ou pela impossibilidade de se disponibilizar de frutas frescas durante as travessias marítimas. A medicina nas caravelas - Século XV, Cristina B. F. M. Gurgel I; Rachel Lewinsohn II, Marujos, Alimentação e Higiene a Bordo
  30. ^ Jacques Cartier's Second Voyage, 1535 Winter & Scurvy.
  31. ^ Martini E (2002). "Jacques Cartier witnesses a treatment for scurvy". Vesalius. 8 (1): 2–6. PMID 12422875. {{cite journal}}: Invalid |ref=harv (help)
  32. ^ Brown, Mervyn. A history of Madagascar. p. 34.
  33. ^ Drymon, M. M. (2008). Disguised As the Devil: How Lyme Disease Created Witches and Changed History. Wythe Avenue Press. p. 114. ISBN 0-615-20061-3.
  34. ^ Lamb, Jonathan (2001). Preserving the self in the south seas, 1680–1840. University of Chicago Press. p. 117. ISBN 0-226-46849-6.
  35. ^ Kerr, Gordon (2009). Timeline of Britain. Canary Press.
  36. ^ Bown, Stephen R. (2003). Scurvy: How a Surgeon, a Mariner and a Gentleman Solved the Greatest Medical Mystery of the Age of Sail. New York: Viking. ISBN 0-312-31391-8.
  37. ^ "Cure for Scurvy discovered by a woman". Telegraph newspaper. 5 March 2009. {{cite news}}: Italic or bold markup not allowed in: |publisher= (help)
  38. ^ Bartholomew, Michael (2002). "James Lind and scurvy: A revaluation". Journal for Maritime Research. 4 (1): 1–14. doi:10.1080/21533369.2002.9668317. PMID 20355298. Retrieved February 16, 2015.
  39. ^ Johann Friedrich Bachstrom, Observationes circa scorbutum [Observations on scurvy] (Leiden ("Lugdunum Batavorum"), Netherlands: Conrad Wishof, 1734) p. 16. From page 16: " … sed ex nostra causa optime explicatur, quae est absentia, carentia & abstinentia a vegetabilibus recentibus, … " ( … but [this misfortune] is explained very well by our [supposed] cause, which is the absence of, lack of, and abstinence from fresh vegetables, … )
  40. ^ "The Blood of Nelson" by Glenn Barnett — Military History — Oct 2006.
  41. ^ Bartholomew, M (Jan 2002). "James Lind and Scurvy: a Revaluation". Journal for Maritime Research.
  42. ^ "Captain Cook and the Scourge of Scurvy" BBC – History
  43. ^ A. S. Turberville (2006). "Johnson's England: An Account of the Life & Manners of His Age". ISBN READ BOOKS. p.53. ISBN 1-4067-2726-1
  44. ^ Vale and Edwards (2011). Physician to the Fleet; the Life and Times of Thomas Trotter 1760-1832. Woodbridge: The Boydell Press. pp. 29–33. ISBN 978 1 84383 604 9.
  45. ^ Stubbs, B. J. (2003). "Captain Cook's Beer; the anti-scorbutic effects of malt and beer in late 18th century sea voyages". Asia and Pacific Journal of Clinical Nutrition. 12 (2): 129–37. PMID 12810402.
  46. ^ Fernandez-Armesto, Felipe (2006). Pathfinders: A Global History of Exploration. W.W. Norton & Company. p. 297. ISBN 0-393-06259-7.
  47. ^ BBC  — History — Captain Cook and the Scourge of Scurvy.
  48. ^ Fernandez-Armesto, Felipe (2006). Pathfinders: A Global History of Exploration. W.W. Norton & Company. pp. 297–298. ISBN 0-393-06259-7.
  49. ^ Blane, Gilbert (1785). Observations on the diseases incident to seamen. London: Joseph Cooper; Edinburgh: William Creech
  50. ^ Thomas Trotter; Francis Milman (1786). Observations on the Scurvy: With a Review of the Theories Lately Advanced on that Disease ; and the Opinions of Dr Milman Refuted from Practice. Charles Elliott and G.G.J. and J. Robinson, London.
  51. ^ Vale, Brian (2008). "The Conquest of Scurvy in the Royal Navy 1793–1800: a Challenge to Current Orthodoxy". The Mariner's Mirror. 94: 160–175. doi:10.1080/00253359.2008.10657052.
  52. ^ Larrey is quoted in French by Dr. Béraud, Études Hygiéniques de la chair de cheval comme aliment, Musée des Familles (1841-42).
  53. ^ Simpson, J.; Weiner, E. (1989). The Oxford English Dictionary. Oxford University Press.
  54. ^ Mabey, Richard (1972). Food for free. Collins. pp. 93, 94. ISBN 978-0-00-724768-4.
  55. ^ Scott, Robert F. (1905). The Voyage of the Discovery. London: Smith, Elder & Co. p. 550. I understand that scurvy is now believed to be ptomaine poisoning
  56. ^ Scott, Robert F. (1905). The Voyage of the Discovery. London: Smith, Elder & Co. p. 556. [no] party wintering in the Antarctic Regions will have great difficulty in providing themselves with fresh food; and, as we have proved, where such conditions exist there need be no fear of the dreaded word 'scurvy'.
  57. ^ Norum KR, Grav HJ (June 2002). "[Axel Holst and Theodor Frolich--pioneers in the combat of scurvy]". Tidsskr. Nor. Laegeforen. 122 (17): 1686–7. PMID 12555613.
  58. ^ McClellan Walter S., Du Bois Eugene F. (1930). "Prolonged meat diet experiment" (PDF). J Biol Chem. 87: 651–668.
  59. ^ Carpenter, Kenneth J. (2004-06-22). "The Nobel Prize and the Discovery of Vitamins". http://www.nobelprize.org. Nobel Foundation. Retrieved 2008-01-25. {{cite web}}: External link in |work= (help)
  60. ^ "The Albert Szent-Gyorgyi Papers Szeged, 1931-1947: Vitamin C, Muscles, and WWII". https://profiles.nlm.nih.gov/. U.S. National Library of Medicine. Retrieved 2008-01-25. {{cite web}}: External link in |work= (help)
  61. ^ Is scurvy making a comeback?, BBC News, 2016
  62. ^ Scurvy makes surprise return in Australia, BBC News, 2016
  63. ^ Pemberton, J. (2006). "Medical experiments carried out in Sheffield on conscientious objectors to military service during the 1939–45 war". International Journal of Epidemiology. 35 (3): 556–558. doi:10.1093/ije/dyl020. PMID 16510534.
  64. ^ Hodges, R. E.; Baker, E. M.; Hood, J.; Sauberlich, H. E.; March, S. C. (1969). "Experimental Scurvy in Man". American Journal of Clinical Nutrition. 22 (5): 535–548. PMID 4977512.
  65. ^ Cueto GR, Allekotte R, Kravetz FO (2000). "[Scurvy in capybaras bred in captivity in Argentine.]". J Wildl Dis. 36 (1): 97–101. doi:10.7589/0090-3558-36.1.97. PMID 10682750.
  66. ^ "Vitamin C". Food Standards Agency (UK). Retrieved 2007-02-19.
  67. ^ "Vitamin C". University of Maryland Medical Center. January 2007. Retrieved 2008-03-31.
  68. ^ Higdon, Jane, Ph.D. (2006-01-31). "Vitamin C". Oregon State University, Micronutrient Information Center. Retrieved 2007-03-07.{{cite web}}: CS1 maint: multiple names: authors list (link)
  69. ^ Evans PR (December 1983). "Infantile scurvy: the centenary of Barlow's disease". Br Med J (Clin Res Ed). 287 (6408): 1862–3. doi:10.1136/bmj.287.6408.1862. PMC 1550031. PMID 6423046. {{cite journal}}: Invalid |ref=harv (help)
  70. ^ Carpenter, Kenneth J. (1988). The History of Scurvy and Vitamin C. Cambridge University Press. p. 172. ISBN 0-521-34773-4.

Further reading

  • Media related to Scurvy at Wikimedia Commons
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