Dairying barriers affect the distribution of lactose malabsorption

Most mammals stop drinking milk at weaning, which is also the time when they cease producing lactase, the digestive enzyme that hydrolyzes lactose. Cessation of lactase production and milk drinking also characterize most human populations, especially those of African and Asian descent. However, a genetic mutation that maintains the functionality of lactase production into adulthood occurs commonly among populations from northern Europe, where dairying is practiced routinely. Indeed, the ability to absorb lactose is nutritionally beneficial for adults only if milk consistently is available. What determines the distribution of dairying? We hypothesized that specific environmental circumstances affect where milk-producing ungulates can be raised safely and economically, thus influencing the geographical occurrence of dairying and lactase persistence. To evaluate this hypothesis, we compiled data on adult lactose absorption (LA) and malabsorption (LM) frequencies in 270 indigenous African and Eurasian populations (Appendix A). Partial correlation analyses revealed that, as predicted, adult LM is associated with extreme climates (at high and low latitudes) and, more significantly, with the historical (pre-1900) geographical occurrence of nine deadly, communicable diseases of cattle. These results suggest that areas where adult LM predominates are those where it is impossible or dangerous to maintain dairy herds.

[1]  J. Cox,et al.  [Lactose intolerance in adults in central Africa]. , 1973, Annales de la Societe belge de medecine tropicale.

[2]  Adel A. F. Mahmoud,et al.  Tropical and Geographical Medicine , 1984 .

[3]  C. S. Seah,et al.  Lactose intolerance in Singapore. , 1970, Gastroenterology.

[4]  F. Simoons,et al.  Primary adult lactose intolerance and the milking habit: A problem in biological and cultural interrelations , 1969, The American Journal of Digestive Diseases.

[5]  A. Dahlqvist,et al.  LACTOSE INTOLERANCE AND PROTEIN MALNUTRITION , 1971, Acta paediatrica Scandinavica.

[6]  E. Winterfeldt,et al.  Lactose intolerance among Mexican Americans. , 1975, The American journal of clinical nutrition.

[7]  G. Keusch,et al.  Normal absorption in Thai subjects with non-specific jejunal abnormalities. , 1967, British medical journal.

[8]  C. Halsted,et al.  Small intestinal structure and absorption in Egypt. Influence of parasitism and pellagra. , 1969, American Journal of Clinical Nutrition.

[9]  R. Bayoumi,et al.  Beja and Nilotes: nomadic pastoralist groups in the Sudan with opposite distributions of the adult lactase phenotypes. , 1982, American journal of physical anthropology.

[10]  D. Swallow,et al.  The genetic polymorphism of intestinal lactase activity in adult humans , 2000 .

[11]  T. Bolin,et al.  Lactose intolerance in Australian-born Chinese. , 1970, Australasian annals of medicine.

[12]  C. Colombo,et al.  Primary lactase deficiency and past malarial endemicity in Sardinia. , 1998, Italian journal of gastroenterology and hepatology.

[13]  C. Snook,et al.  Lactose tolerance in adult Jordanian Arabs. , 1976, Tropical and geographical medicine.

[14]  T. Bayless,et al.  Relationship of milk consumption to blood glucose rise in lactose intolerant individuals. , 1975, The American journal of clinical nutrition.

[15]  G. Cook,et al.  High intestinal lactase concentrations in adult Arbs in Saudi Arabia. , 1975, British medical journal.

[16]  G. Flatz,et al.  Evidence against nutritional adaption of tolerance to lactose , 2004, Humangenetik.

[17]  Charles R.scriver,et al.  The Metabolic basis of inherited disease , 1989 .

[18]  N. Kretchmer,et al.  Lactose malabsorption among the Pima indians of Arizona. , 1977, Gastroenterology.

[19]  B. Senewiratne,et al.  Intestinal lactase deficiency in Ceylon (Sri Lanka). , 1977, Gastroenterology.

[20]  M. Sadre,et al.  Lactose intolerance in Iran. , 1979, The American journal of clinical nutrition.

[21]  M. Lévy,et al.  Lactase deficiency in Mexican-American males. , 1972, The American journal of clinical nutrition.

[22]  Richard A. King,et al.  The genetic basis of common diseases. , 2002 .

[23]  L L Cavalli-Sforza,et al.  Analytic review: some current problems of human population genetics. , 1973, American journal of human genetics.

[24]  H. Delbrück,et al.  Persistence of high intestinal lactase activity (lactose tolerance) in Afghanistan , 1976, Human Genetics.

[25]  G. Flatz The Genetic Polymorphism of Adult Intestinal Lactase Activity , 1991 .

[26]  L. Hussein,et al.  Distribution of human adult lactose phenotypes in Egypt. , 1982, Human heredity.

[27]  J. Haworth,et al.  Intestinal lactase deficiency among east Indians. An adaptive rather than a genetically inherited phenomenon? , 1970, The American journal of gastroenterology.

[28]  E. Melgar,et al.  Intestinal lactase deficiency in an apparently normal Peruvian population , 1971, The American Journal of Digestive Diseases.

[29]  N. Kretchmer,et al.  Lactose malabsorption among adult Indians of the Great Basin and American Southwest. , 1978, The American journal of clinical nutrition.

[30]  G. Neale The diagnosis, incidence and significance of disacchridase deficiency in adults , 1968 .

[31]  G. Flatz,et al.  Lactose Tolerance in Asians: a Family Study , 1969, Nature.

[32]  H. Rotthauwe,et al.  Die Häufigkeit der Lactose-Intoleranz bei gesunden Erwachsenen in Deutschland1, 2 , 1972 .

[33]  Y. Yoshida,et al.  Studies on the etiology of milk intolerance in Japanese adults , 2007, Gastroenterologia Japonica.

[34]  E. Balanza,et al.  The frequency of lactase phenotypes in Aymara children. , 1985, Journal of medical genetics.

[35]  J. Jussila Milk intolerance and lactose malabsorption in hospital patients and young servicemen in Finland. , 1969, Annals of clinical research.

[36]  S. Povey,et al.  Lactase polymorphism in adult British natives: estimating allele frequencies by enzyme assays in autopsy samples. , 1982, American journal of human genetics.

[37]  N. Asp,et al.  Intestinal disaccharidases in Greenland Eskimos. , 1975, Scandinavian journal of gastroenterology.

[38]  P. Lovejoy Pastoralism in Africa , 1979 .

[39]  R. Lisker,et al.  Lactase deficiency in a rural area of Mexico. , 1974, The American journal of clinical nutrition.

[40]  Derek F. Hayward,et al.  Climatology of West Africa , 1987 .

[41]  T. Bolin,et al.  Asian Lactose Intolerance and its Relation to Intake of Lactose , 1969, Nature.

[42]  M. Gracey,et al.  Lactose malabsorption in Australian Aborigines. , 1983, American Journal of Clinical Nutrition.

[43]  T. Bayless,et al.  A racial difference in incidence of lactase deficiency. A survey of milk intolerance and lactase deficiency in healthy adult males. , 1966, JAMA.

[44]  H. Shwachman,et al.  Correlation of lactase activity, lactose tolerance and milk consumption in different age groups. , 1975, The American journal of clinical nutrition.

[45]  E. Zuccato,et al.  Respiratory excretion of hydrogen and methane in Italian subjects after ingestion of lactose and milk , 1983, European journal of clinical investigation.

[46]  F. Simoons,et al.  Geography and genetics as factors in the psychobiology of human food selection. , 1982 .

[47]  S. Kajubi,et al.  Tribal incidence of lactase deficiency in Uganda. , 1966, Lancet.

[48]  A. Hofmann,et al.  Lactase deficiency: a common genetic trait of the American Indian. , 1977, Gastroenterology.

[49]  H. Spiro,et al.  Lactose intolerance in Jewish patients with ulcerative colitis , 1971, The American Journal of Digestive Diseases.

[50]  D. McGill,et al.  Disaccharidase activity in the small intestine: prevalence of lactase deficiency in 100 healthy subjects. , 1967, Gastroenterology.

[51]  C. Kl,et al.  Lactose intolerance: hereditary or acquired? Effect of prolonged milk feeding. , 1973 .

[52]  C. Woteki,et al.  Lactose malabsorption in Mexican-American adults. , 1977, The American journal of clinical nutrition.

[53]  D. Calloway,et al.  Determination of lactose intolerance by breath analysis , 1969, The American Journal of Digestive Diseases.

[54]  S. Auricchio,et al.  High frequency of lactase activity deficiency in small bowel of adults in the Neapolitan area. , 1970, Enzymologia biologica et clinica.

[55]  N. Kretchmer,et al.  A genetic study of lactose digestion in Nigerian families. , 1975, Gastroenterology.

[56]  G. Flatz,et al.  Distribution of physiological adult lactase phenotypes, lactose absorber and malabsorber, in Germany , 2004, Human Genetics.

[57]  G. Neale Defects of Sugar Absorption , 1968, Proceedings of the Royal Society of Medicine.

[58]  J. Rhodes,et al.  Lactase and other disaccharidase deficiencies in a hospital population. , 1968, Israel journal of medical sciences.

[59]  A. Baseer,et al.  High intestinal lactase concentration in adult Pakistanis. , 1976, British medical journal.

[60]  T. Jenkins,et al.  Persistent high intestinal lactase activity in Papua New Guinea. Lactose absorption curves in two populations. , 1981, Annals of human biology.

[61]  N. Asp,et al.  Activities of brush border lactase, acid -galactosidase, and hetero- -galactosidase in the jejunum of the Zambian African. , 1973, Gastroenterology.

[62]  T. Bayless,et al.  Milk and Lactose Intolerance in Healthy Orientals , 1968, Science.

[63]  G. Flatz,et al.  Distribution of human adult lactase phenotypes in the population of Austria , 2004, Human Genetics.

[64]  K Launiala,et al.  Prevalence of lactose malabsorption in a Finnish rural population. , 1970, Scandinavian journal of gastroenterology.

[65]  D. Habte,et al.  LACTOSE MALABSORPTION IN ETHIOPIAN CHILDREN , 1973, Acta paediatrica Scandinavica.

[66]  F. Simoons,et al.  Primary adult lactose intolerance and the milking habit: A problem in biologic and cultural interrelations , 1970, The American Journal of Digestive Diseases.

[67]  F. Simoons,et al.  Persistence of lactase activity among Northern Europeans: A weighing of evidence for the calcium absorption hypothesis , 2001 .

[68]  Sociedad Española de Patología Digestiva Revista española de las enfermedades del aparato digestivo , 1968 .

[69]  M. Lember,et al.  Lactose malabsorption in Khants in western Siberia. , 1995, Scandinavian journal of gastroenterology.

[70]  E. Shafrir,et al.  Behavior of serum free fatty acids and glucose during lactose tolerance tests. , 1968, Israel journal of medical sciences.

[71]  J. Leichter Lactose tolerance in a Slavic population , 2005, The American Journal of Digestive Diseases.

[72]  K. Jeejeebhoy,et al.  LACTASE DEFICIENCY IN THE ADULT , 1965 .

[73]  J. Pieters,et al.  Lactose malabsorption and milk tolerance in Kenyan school-age children. , 1973, Tropical and geographical medicine.

[74]  A. Dahlqvist,et al.  Jejunal hetero-beta-galactosidase activities in Ugandans with lactase deficiency. , 1968, Gastroenterology.

[75]  T. Bayless,et al.  Lactose malabsorption and milk rejection in Negro children. , 1971, The Johns Hopkins medical journal.

[76]  T. Jenkins,et al.  Public Health and Genetic Constitution of the San (“Bushmen”): Carbohydrate Metabolism and Acetylator Status of the! Kung of Tsumkwe in the North-western Kalahari* , 1974, British medical journal.

[77]  J. Welsh,et al.  Isolated Lactase Deficiency: Correlation of Laboratory Studies and Clinical Data , 1967 .

[78]  A. Dahlqvist,et al.  Specific small-intestinal lactase deficiency in adults. , 1969, Scandinavian journal of gastroenterology.

[79]  C. Woteki,et al.  Lactose malabsorption in Mexican-American children. , 1976, The American journal of clinical nutrition.

[80]  G. Flatz,et al.  Prevalence of primary adult lactose malabsorption in Pakistan. , 1984, Human heredity.

[81]  J. Leichter Lactose tolerance in a jewish population , 1971, The American Journal of Digestive Diseases.

[82]  D. McGill,et al.  Lactase deficiency in Orientals. , 1968, Gastroenterology.

[83]  S. Nasrallah Lactose intolerance in the Lebanese population and in "Mediterranean lymphoma". , 1979, The American journal of clinical nutrition.

[84]  Pardis C Sabeti,et al.  Genetic signatures of strong recent positive selection at the lactase gene. , 2004, American journal of human genetics.

[85]  T. Bayless,et al.  Intolerance of eight ounces of milk in healthy lactose-intolerant teen-agers. , 1975, Pediatrics.

[86]  I. Segal,et al.  Lactase deficiency in the South African black population. , 1983, The American journal of clinical nutrition.

[87]  C. Bartholomew,et al.  Lactose intolerance in East Indians of Trinidad. , 1976, Tropical and geographical medicine.

[88]  A. Valyasevi,et al.  Lactose malabsorption in Thai infants and children: effect of prolonged milk feeding. , 1976, The Southeast Asian journal of tropical medicine and public health.

[89]  G. Flatz,et al.  Distribution of adult lactase phenotypes in the Tuareg of Niger. , 1986, American journal of human genetics.

[90]  Chang Wp,et al.  Lactose tolerance in adult Jordanian Arabs. , 1976 .

[91]  T. Bayless,et al.  Lactose malabsorption in preschool black children. , 1977, The American journal of clinical nutrition.

[92]  J. Pershad,et al.  Lactase deficiency in Indians. , 1972, The American journal of clinical nutrition.

[93]  W. Kuehnau,et al.  Prevalence of primary adult lactose malabsorption in three populations of northern China , 2004, Human Genetics.

[94]  Pieters Jj,et al.  Lactose malabsorption and milk tolerance in Kenyan school-age children. , 1973 .

[95]  C. Scriver,et al.  The Metabolic and Molecular Bases of Inherited Disease, 8th Edition 2001 , 2001, Journal of Inherited Metabolic Disease.

[96]  S. Matri,et al.  Etude de la malabsorption du lactose par le test respiratoire à l'hydrogène dans une population de 70 adultes tunisiens , 1987 .

[97]  T. Gilat,et al.  Lactose tolerance in an Arab population , 1971, The American Journal of Digestive Diseases.

[98]  L. Hussein,et al.  The frequency distribution of lactose malabsorption among adult populations from the Eastern and Western Egyptian Deserts , 1994, Biochemical Genetics.

[99]  T. Sahi,et al.  LACTOSE MALABSORPTION IN FINNISH CHILDREN OF SCHOOL AGE , 1972, Acta paediatrica Scandinavica.

[100]  T. Gilat,et al.  Lactase deficiency in Jewish communities in Israel , 1970, The American Journal of Digestive Diseases.

[101]  C. la Vecchia,et al.  High prevalence of lactose absorbers in Northern Sardinian patients with type 1 and type 2 diabetes mellitus. , 2001, The American journal of clinical nutrition.

[102]  D. Olatunbosun,et al.  Lactase deficiency in Nigerians , 1971, The American Journal of Digestive Diseases.

[103]  E J Hollox,et al.  Lactase haplotype diversity in the Old World. , 2001, American journal of human genetics.

[104]  A. Czeizel,et al.  Prevalence of primary adult lactose malabsorption in Hungary , 2004, Human Genetics.

[105]  J. Książyk,et al.  Prevalence of primary adult lactose malabsorption in Poland. , 1984, Annals of human biology.

[106]  E. Scott,et al.  Lactose intolerance in Alaskan Indians and Eskimos. , 1972, The American journal of clinical nutrition.

[107]  R. McCracken,et al.  Lactase Deficiency: An Example of Dietary Evolution , 1971, Current Anthropology.

[108]  K. Dağalp,et al.  Distribution of the adult lactase phenotypes in Turkey. , 1986, Tropical and geographical medicine.

[109]  R. Whitehead,et al.  Absorption of lactose and its digestion products i the normal and malnourished Ugandan. , 1967, Gut.

[110]  F. Lecocq,et al.  Effect of fasting and refeeding on the histology and disaccharidase activity of the human intestine. , 1968, Gastroenterology.

[111]  N. Anh,et al.  Lactose malabsorption in adult Vietnamese. , 1977, The American journal of clinical nutrition.

[112]  F. Simoons,et al.  The geographic hypothesis and lactose malabsorption , 1978, The American Journal of Digestive Diseases.

[113]  S. Jarnum,et al.  [Lactose malabsorption in West Greenland]. , 1973, Ugeskrift for laeger.

[114]  G. Flatz,et al.  Distribution of adult lactase phenotypes in Bedouins and in urban and agricultural populations of Jordan. , 1983, Tropical and geographical medicine.

[115]  Mustakallio Kk Annals of Clinical Research , 1968 .

[116]  H. Desai,et al.  Incidence of lactase deficiency in control subjects from India. Role of hereditary factors. , 1970, Indian journal of medical sciences.

[117]  D. Johnson The nature of nomadism. , 1969 .

[118]  J. Jersky,et al.  Lactase deficiency in the South African Bantu. , 1967 .

[119]  P. Fottrell,et al.  The incidence of primary hypolactasia amongst native Irish , 1981, Irish journal of medical science.

[120]  J. Jay Braun,et al.  Evolution and Human Behavior , 1967, The Yale Journal of Biology and Medicine.

[121]  H. Alzate,et al.  Lactose intolerance in South American Indians. , 1969, The American journal of clinical nutrition.

[122]  C. Kattamis,et al.  LACTOSE INTOLERANCE IN GREEKS , 1973 .

[123]  S. Odend'hal The Geographical Distribution of Animal Viral Diseases , 1983 .

[124]  J. Cox,et al.  Primary adult lactose intolerance in the Kivu Lake area: Rwanda and the bushi , 1974, The American Journal of Digestive Diseases.

[125]  A. PeñaYáñez,et al.  Lactose malabsorption in Spanish students. I. Intestinal tolerance to an oral load of lactose , 1971 .

[126]  A. Boner,et al.  Prevalence of primary adult lactose malabsorption and awareness of milk intolerance in Italy. , 1984, The American journal of clinical nutrition.

[127]  G. Flatz,et al.  Genetics of lactose digestion in humans. , 1987, Advances in human genetics.

[128]  N. Kretchmer,et al.  Lactose malabsorption: its biology and history. , 1974, Advances in pediatrics.

[129]  G. Keusch,et al.  Lactase deficiency in Thailand: effect of prolonged lactose feeding. , 1969, The American journal of clinical nutrition.

[130]  N. Kretchmer,et al.  Intestinal absorption of lactose in Nigerian ethnic groups. , 1971, Lancet.

[131]  G. Rosa,et al.  HIGH FREQUENCY OF LACTOSE ABSORBERS AMONG ADULTS WITH IDIOPATHIC SENILE AND PRESENILE CATARACT IN A POPULATION WITH A HIGH PREVALENCE OF PRIMARY ADULT LACTOSE MALABSORPTION , 1984, The Lancet.

[132]  H. Delbrück,et al.  Distribution of the adult lactase phenotypes--lactose absorber and malabsorber--in a group of 131 army recruits. , 1982, Gastroentérologie Clinique et Biologique.

[133]  J. Welsh,et al.  Lactose malabsorption in Oklahoma Indians. , 1973, The American journal of clinical nutrition.

[134]  J. Curry,et al.  Encyclopedia of atmospheric sciences , 2002 .

[135]  E. B. Kraus,et al.  Atmosphere-Ocean Interaction , 1972 .

[136]  T. Sahi,et al.  Lactose malabsorption in school-children. , 1971, Acta paediatrica Scandinavica.

[137]  G. Flatz,et al.  Lactose Intolerance in Thailand , 1969, Nature.

[138]  T. Sahi Lactose malabsorption in Finnish-speaking and Swedish-speaking populations in Finland. , 1974, Scandinavian journal of gastroenterology.

[139]  J. Coetzer,et al.  Infectious diseases of livestock with special reference to Southern Africa: Volume 1. , 1994 .

[140]  J. Leichter,et al.  Lactose intolerance in Canadian West Coast Indians , 1971, The American Journal of Digestive Diseases.

[141]  R. Luyken,et al.  Lactose intolerance in Surinam. , 1971, Maandschrift voor kindergeneeskunde.

[142]  N. Danos,et al.  Primary lactase deficiency in Greek adults , 1974, The American Journal of Digestive Diseases.

[143]  G. Flatz,et al.  Lactose intolerance in Arabs , 1971, Humangenetik.

[144]  V. Binder,et al.  The incidence of lactose malabsorption in ulcerative colitis. , 1975, Scandinavian journal of gastroenterology.

[145]  F. Simoons The Antiquity of Dairying in Asia and Africa , 1971 .

[146]  T. Gilat,et al.  Genetics of primary adult lactase deficiency. , 1973, Gastroenterology.

[147]  K. Hirschhorn,et al.  Advances in Human Genetics , 1982, Springer US.

[148]  T. Gilat,et al.  Lactase in childhood--a non-adaptable enzyme. , 1974, Scandinavian journal of gastroenterology.

[149]  John F. Griffiths,et al.  Climates of Africa , 1972 .

[150]  R. Bayoumi,et al.  Distribution of the lactase phenotypes in the population of the Democratic Republic of the Sudan , 2004, Human Genetics.