Management of diarrhea and nutritional support

HIV infection in children is often thought to be a rapidly and uniformly lethal disease. In Rwanda, however, 40% of children with perinatal infection survive for 5 years without antiretroviral treatment, and there are many children in sub-Saharan Africa with vertically acquired HIV infection attending schools and growing into adoles-cence.112 Optimizing the quality of life for these children is a necessary challenge, especially when the option of effective antiretroviral therapy is absent. The approaches outlined below are intended for developing countries.

Diarrhea

In most clinical settings in southern Africa it is not possible to investigate children presenting with recurrent or persistent diarrhea extensively. Using a syndromic approach for managing diarrhea in both HIV-infected and uninfected children is therefore appropriate. The WHO/UNICEF Integrated Management of Childhood Illnesses (IMCI) recommends that children with a history of persistent diarrhea and/or reported weight loss in the previous 3 months should be assessed for possible HIV infection.113 Where there are no specific guidelines for HIV-infected children, the WHO guidelines for the management of severe malnutrition, including persistent diarrhea, are helpful.

An approach for resource-poor countries would be:

  • 1) Assess for and correct dehydration, hypo-glycemia, hypothermia and electrolyte disturbances, especially K+ deficiency;
  • 2) Treat concurrent bacterial infections, e.g. pneumonia, Pneumocystis carinii pneumonia (PCP) and urinary tract infection, and exclude TB. This often means giving antibiotics empirically, e.g. cefuroxime, gentamycin and cotri-moxazole;
  • 3) Start low lactose (< 3.2 g/kg) containing feeds such as F-75 (WHO) and porridge;
  • 4) Provide vitamin A, zinc and multivitamins, including folate. See below for comment on zinc supplements;
  • 5) If diarrhea persists then test stools for lactose intolerance using Clinitest┬« tablets;
  • 6) If Clinitest is positive then exclude all lactose from diet - use milks containing maltodextran as the main carbohydrate;
  • 7) If Clinitest is negative then send repeat stools for routine microbiological assessment, including for Shigella, non-typhi Salmonella, Cryptosporidium, microsporidia and TB. Treat accordingly. Cryptosporidia may be shed intermittently; three stools should be sent to exclude diagnosis. Experienced staff are required to identify cryptosporidia and microsporidia on routine stool analysis. Prolonged fluid and nutritional support is often required for patients with cryp-tosporidiosis;
  • 8) If no pathogen is identified then treat for bacterial overgrowth, e.g. cholestyramine for 5 days and neomycin for 3 days;
  • 9) If diarrhea persists check for monosaccharide intolerance; test for glucose in stool using Clinitest or Glucostix┬«. If positive, check for excessive intake of oral rehydration solution (ORS). Use maltodextran (glucose polymer) containing feeds and deliver milk by continuous slow infusion through a nasogastric tube. Use plain boiled water for oral rehydration rather than ORS. Only revert back to bolus feeds once the stool becomes formed again and glucose is not present. This takes longer in children who are more wasted or who have severe diarrhea;
  • 10) Where resources are available, perform upper gastrointestinal endoscopy to increase the microbiological diagnostic yield. If visible or microscopic blood is present in stools then perform sigmoidoscopy for biopsy and culture;

Management of diarrhea and nutritional support 121

  • 11) Where there is persistent pyrexia consider CMV colitis and exclude TB;
  • 12) If no cause for persisting diarrhea is evident then consider antimotility drugs such as loperamide (HIV enteropathy is a diagnosis of exclusion);
  • 13) Older children should be asked about abdominal pain and on these occasions underlying opportunistic infections such as TB, Cryptosporidium or CMV should be excluded; opiates such as codeine phosphate may be helpful;
  • 14) Attention must be given in the weeks following discharge to restoring, as much as possible, any weight loss that has occurred. It is often very difficult to achieve this during hospitalization, and in busy hospitals significant weight gain cannot be used as a criterion for discharge (see Nutrition, below).

Parenteral nutrition is not generally feasible in most developing countries because of the risk of systemic infection and metabolic complications.

Terminal care

When children are admitted with evidence of clinically advanced HIV infection such as diarrhea and severe wasting, clinicians and carers must consider what is reasonable and right for the child. The first admission with diarrhea often results in HIV testing. Many mothers discover for the first time that both she, and her child, are HIV-infected. In this situation it is appropriate to use all resources available to ensure that the child recovers and is able to go home. However, the treatment paradigm and objectives for care often change when the child has suffered several admissions, and the family has had some time to adapt to the diagnosis. In the absence of antiviral drugs, relieving discomfort becomes the overriding priority, and being less aggressive when complications such as concurrent severe bacterial infections intervene may be more caring for the child.

In resourced settings

While the same principles apply, the use of invasive diagnostic methods, i.e. upper and lower intestinal endoscopy, should be used early to determine whether a treatable enteric pathogen is present. Parenteral feeding may be a safe option if severe malabsorption is present. Antiretroviral drugs should be initiated if the child has not been previously treated.

Micronutrients and HIV-related diarrhea

Multiple micronutrient deficiencies have been reported in both HIV-infected adults and children with, or without, diarrhea. Biochemical indicators of vitamin and trace element status may be misleading and reflect redistribution or acute-phase responses rather true body depletion. A few studies have shown that micronutrient supplementation in HIV-infected or exposed children is associated with improved morbidity or immune function.114-116 In children uninfected with HIV, zinc supplementation reduces the incidence, duration and severity of acute and chronic diarrhea and promotes recovery of the mucosal lining.117,118 This effect has not so far been demonstrated in HIV-infected children.

Vitamin A does not seem significantly to influence the course of acute or persistent diarrhea in un-infected children, but does decrease the severity and likelihood of recurrence.119 HIV-infected children with persistent diarrhea should receive vitamin A (0-6 months, 50 000IU; 6-12 months, 100 000 IU; >12 months, 200000IU daily for 2 days), zinc sulfate or gluconate 2 mg/kg for 2 weeks and multivitamin preparations including folate for 2-4 weeks.

Nutrition

Much of the impact of diarrheal illnesses and repeated opportunistic infections on the health of HIV-infected children is mediated by its effect on nutrition. Loss of lean body tissue is consistently seen in adults and children with advanced disease and is a strong predictor of death.120 Resting energy expenditure (REE) in adults increases by about 10% once they are infected with HIV, but this does not been seem to be the case in children.53,121 However, even if REE increases modestly, total energy expenditure may not increase, because of inactivity. Rather, weight loss is most likely to be due to decreased energy intake, especially during the recovery period from opportunistic infections. Nutritional interventions, however, have generally only reversed weight loss through gain of fat rather than lean body tissue. There is work to suggest that different opportunistic infections may have differential effects on nutrition with some being capable of impairing anabolism and effective utilization of energy from food.

WHO currently recommends that infected children should increase their overall energy intake by about 10% in order to maintain normal health, growth and activity. In chronic illness such as TB infection or chronic lung disease, energy intake should increase by 25-30%. During acute illnesses, particularly when recovering from acute weight loss, these requirements may increase to 50-100% extra energy. Protein should represent about 10-15% of energy. These goals should ideally be achieved through dietary approaches rather than by specialized supplements which may not be available or affordable in most developing countries.122

Surgical aspects of HIV infection

The prevalence of HIV disease among pediatric surgical patients in southern Africa has increased dramatically and is frequently considered as part of the differential diagnosis. Abdominal pain is not uncommon in adults with HIV, but there are no data on children. An underlying pathological cause can be identified in most cases123 and include TB abdomen, cryptosporidia and CMV. There are four common surgical manifestations of gastrointestinal HIV disease: destructive lesions, opportunistic infections, primary peritonitis and tumors.

Destructive lesions

Rectovaginal fistulae are an extremely common presentation of HIV disease in female infants.124,125 In the past this was treated with a defunctioning colostomy followed by closure of the fistula. Recurrence was frequent. Antiretroviral therapy may improve surgical results, but in the absence of such treatment it is generally better to leave the fistula alone.126 In males, there is the less common presentation of a rectourethral fistula which always requires surgical repair.

Occasionally stricture formation may follow sclerosis of the lower esophagus after repeated ulcerative disease such as CMV or invasive candidiasis.

Opportunistic infections

Intestinal perforations due to CMV are described above.104 HIV occasionally presents as cancrum oris, where early treatment with penicillin and metronidazole may help, but excision and reconstruction may be required for large areas of full-thickness skin and tissue loss.

Primary peritonitis

This is sometimes seen in the older child who presents with a clinical picture suggestive of appendicitis. At surgery an odorless pus is found in the abdomen; pneumococcus is often isolated.

Tumors

Kaposi's sarcoma in the gut may present with rectal bleeding, and other less common smooth-muscle tumors may rarely present as an intussusception and intestinal obstruction.127,128

Condyloma accuminata that may vary in size from isolated lesions to large pancake lesions can cover the perineum and genitalia. The more extensive lesions cause severe discomfort and problems with local hygiene. Isolated lesions may respond to podophyllin, but diathermy results in annular scarring and anal stenosis. Treatment with interferon may be helpful.

Sialadenitis is a frequent complaint. Parotid size may increase and decrease intermittently, and pain may be due to superimposed bacterial infection, TB, bleeding into cysts or malignant change. Acute pain should be treated with antibiotics and analgesia; if the parotid continues to enlarge and is painful, then fine-needle or open biopsy should be performed to exclude TB or malignant change. Corticosteroids may be helpful.

REFERENCES

  1. McDougal JS, Mawle A, Cort SP et al. Cellular tropism of the human retrovirus HTLV-III/LAV. I. Role of T cell activation and expression of the T4 antigen. J Immunol 1985; 135: 3151-3162.
  2. Lapenta C, Boirivant M, Marini M et al. Human intestinal lamina propria lymphocytes are naturally permissive to HIV-1 infection. Eur J Immunol 1999; 29: 1202-1208.
  3. Rollins NC, Filteau SM, Coutsoudis A, Tomkins AM. Feeding mode, intestinal permeability, and neopterin excretion: a longitudinal study in infants of HIV-infected South African women. J Acquir Immune Defic Syndr 2001; 28: 132-139.
  4. Meng G, Wei X, Wu X et al. Primary intestinal epithelial cells selectively transfer R5 HIV-1 to CCR5+ cells. Nat Med 2002; 8: 150-156.
  5. Poles MA, Elliott J, Taing P et al. A preponderance of CCR5(+) CXCR4(+) mononuclear cells enhances gastrointestinal mucosal susceptibility to human immunodeficiency virus type 1 infection. J Virol 2001; 75: 8390-8399.
  6. Wolinsky SM, Wike CM, Korber BT et al. Selective transmission of human immunodeficiency virus type-1 variants from mothers to infants. Science 1992; 255: 1134-1137.
  7. Amerongen HM, Weltzin R, Farnet CM et al. Transepithelial transport of HIV-1 by intestinal M cells: a mechanism for transmission of AIDS. J Acquir Immune Defic Syndr 1991; 4: 760-765.
  8. Dunn DT, Newell ML, Ades AE, Peckham CS. Risk of human immunodeficiency virus type 1 transmission through breastfeeding. Lancet 1992; 340: 585-588.
  9. Lewis P, Nduati R, Kreiss JK et al. Cell-free human immunodeficiency virus type 1 in breast milk. J Infect Dis 1998; 177: 34-39.
  10. Leroy V, Karon JM, Alioum A et al. Postnatal transmission of HIV-1 after a maternal short-course zidovudine peripartum regimen in West Africa. AIDS 2003; 17: 1493-1501.
  11. Hocini H, Bomsel M. Infectious human immunodeficiency virus can rapidly penetrate a tight human epithelial barrier by transcytosis in a process impaired by mucosal immunoglobulins. J Infect Dis 1999; 179(Suppl 3): S448-S453.
  12. McNeely TB, Dealy M, Dripps DJ et al. Secretory leukocyte protease inhibitor: a human saliva protein exhibiting anti-human immunodeficiency virus 1 activity in vitro. J Clin Invest 1995; 96: 456-464.
  13. Janoff EN, Scamurra RW, Sanneman TC et al. Human immunodeficiency virus type 1 and mucosal humoral defense. J Infect Dis 1999; 179(Suppl 3): S475-S479.
  14. Willumsen JF, Filteau SM, Coutsoudis A et al. Breastmilk RNA viral load in HIV-infected South African women: effects of subclinical mastitis and infant feeding. AIDS 2003; 17: 407-414.
  15. Fearon DT, Locksley RM. The instructive role of innate immunity in the acquired immune response. Science 1996; 272: 50-53.
  16. Medzhitov R, Janeway CA Jr. Innate immunity: impact on the adaptive immune response. Curr Opin Immunol 1997; 9: 4-9.
  17. Kalliomaki M, Salminen S, Arvilommi H et al. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 2001; 357: 1076-1079.
  18. Devito C, Broliden K, Kaul R et al. Mucosal and plasma IgA from HIV-1-exposed uninfected individuals inhibit HIV-1 transcytosis across human epithelial cells. J Immunol 2000; 165: 5170-5176.
  19. Alfsen A, Iniguez P, Bouguyon E, Bomsel M. Secretory IgA specific for a conserved epitope on gp41 envelope glycoprotein inhibits epithelial transcytosis of HIV-1. J Immunol 2001; 166: 6257-6265.
  20. Veazey RS, Shattock RJ, Pope M et al. Prevention of virus transmission to macaque monkeys by a vaginally applied monoclonal antibody to HIV-1 gp120. Nat Med 2003; 9: 343-346.
  21. Lim SG, Condez A, Lee CA et al. Loss of mucosal CD4 lymphocytes is an early feature of HIV infection. Clin Exp Immunol 1993; 92: 448-454.
  22. Schneider T, Jahn HU, Schmidt W et al. Loss of CD4 T lymphocytes in patients infected with human immunodeficiency virus type 1 is more pronounced in the duodenal mucosa than in the peripheral blood. Berlin Diarrhea/Wasting Syndrome Study Group. Gut 1995; 37: 524-529.
  23. Clayton F, Snow G, Reka S, Kotler DP. Selective depletion of rectal lamina propria rather than lymphoid aggregate CD4 lymphocytes in HIV infection. Clin Exp Immunol 1997; 107: 288-292.
  24. Kotler DP, Scholes JV, Tierney AR. Intestinal plasma cell alterations in acquired immunodeficiency syndrome. Dig Dis Sci 1987; 32: 129-138.
  25. Schneider T, Zippel T, Schmidt W et al. Secretory immunity in HIV infection. Pathobiology 1998; 66: 131-138.
  26. Kakai R, Bwayo JJ, Wamola IA et al. Effect of human immunodeficiency virus on local immunity in children with diarrhoea. East Afr Med J 1995; 72: 699-702.
  27. Bard E, Laibe S, Clair S et al. Nonspecific secretory immunity in HIV-infected patients with oral candidiasis. J Acquir Immune Defic Syndr 2002; 31: 276-284.
  28. Chadwick EG, Chang G, Decker MD et al. Serologic response to standard inactivated influenza vaccine in human immunodeficiency virus-infected children. Pediatr Infect Dis J 1994; 13: 206-211.
  29. Olsson J, Poles M, Spetz AL et al. Human immunodeficiency virus type 1 infection is associated with significant mucosal inflammation characterized by increased expression of CCR5, CXCR4, and beta-chemokines. J Infect Dis 2000; 182: 1625-1635.
  30. Bode H, Schmitz H, Fromm M et al. IL-1beta and TNF-alpha, but not IFN-alpha, IFN-gamma, IL-6 or IL-8, are secretory mediators in human distal colon. Cytokine 1998; 10: 457-465.
  31. Colebunders R, Francis H, Mann JM et al. Persistent diarrhea, strongly associated with HIV infection in Kinshasa, Zaire. Am J Gastroenterol 1987; 82: 859-864.
  32. Chintu C, DuPont HL, Kaile T et al. Human immunodeficiency virus-associated diarrhea and wasting in Zambia: selected risk factors and clinical associations. Am J Trop Med Hyg 1998; 59: 38-41.
  33. Monkemuller KE, Call SA, Lazenby AJ, Wilcox CM. Declining prevalence of opportunistic gastrointestinal disease in the era of combination antiretroviral therapy. Am J Gastroenterol 2000; 95: 457-462.
  34. Nannini EC, Okhuysen PC. HIV1 and the gut in the era of highly active antiretroviral therapy. Curr Gastroenterol Rep 2002; 4: 392-398.

Kotler DP, Francisco A, Clayton F et al. Small intestinal injury and parasitic diseases in AIDS. Ann Intern Med 1990; 113: 444-449.

Carbonnel F, Beaugerie L, Abou RA et al. Macronutrient intake and malabsorption in HIV infection: a comparison with other malabsorptive states. Gut 1997; 41: 805-810.

Yolken RH, Hart W, Oung I et al. Gastrointestinal dysfunction and disaccharide intolerance in children infected with human immunodeficiency virus. J Pediatr 1991; 118: 359-363.

Miller TL, Orav EJ, Martin SR et al. Malnutrition and carbohydrate malabsorption in children with vertically transmitted human immunodeficiency virus 1 infection. Gastroenterology 1991; 100: 1296-1302. The Italian Paediatric Intestinal/HIV Study Group. Intestinal malabsorption of HIV-infected children: relationship to diarrhoea, failure to thrive, enteric microorganisms and immune impairment. AIDS 1993; 7: 1435-1440.

Lepage P, Spira R, Kalibala S et al. Care of human immunodeficiency virus-infected children in developing countries. International Working Group on Mother-to-Child Transmission of HIV. Pediatr Infect Dis J 1998; 17: 581-586.

Keating J, Bjarnason I, Somasundaram S et al. Intestinal absorptive capacity, intestinal permeability and jejunal histology in HIV and their relation to diarrhoea. Gut 1995; 37: 623-629.

Kotler DP, Reka S, Chow K, Orenstein JM. Effects of enteric parasitoses and HIV infection upon small intestinal structure and function in patients with AIDS. J Clin Gastroenterol 1993; 16: 10-15. Fontana M, Boldorini R, Zuin G et al. Ultrastructural changes in the duodenal mucosa of HIV-infected children. J Pediatr Gastroenterol Nutr 1993; 17: 255-259. Thea DM, St Louis ME, Atido U et al. A prospective study of diarrhea and HIV-1 infection among 429 Zairian infants. N Engl J Med 1993; 329: 1696-1702. Miller TL, McQuinn LB, Orav EJ. Endoscopy of the upper gastrointestinal tract as a diagnostic tool for children with human immunodeficiency virus infection. J Pediatr 1997; 130: 766-773.

Oktedalen O, Skar V, Dahl E, Serck-Hanssen A. Changes in small intestinal structure and function in HIV-infected patients with chronic diarrhoea. Scand J Infect Dis 1998; 30: 459-463.

Pernet P, Vittecoq D, Kodjo A et al. Intestinal absorption and permeability in human immunodeficiency virus-infected patients. Scand J Gastroenterol 1999; 34: 29-34. Taylor C, Hodgson K, Sharpstone D et al. The prevalence and severity of intestinal disaccharidase deficiency in human immunodeficiency virus-infected subjects. Scand J Gastroenterol 2000; 35: 599-606. Rollins NC, Wittenberg DF, Coovadia HM. Trends in HIV prevalence outcome and monosaccharide intolerance in a paediatric diarrhoea unit in South Africa. Commonwealth Congress on Diarrhoea and Malnutrition, Karachi, Pakistan, 1997. Sharpstone D, Neild P, Crane R et al. Small intestinal transit, absorption, and permeability in patients with AIDS with and without diarrhoea. Gut 1999; 45: 70-76. Kotler D, Haroutiounian G, Greenberg R. Increased bile salt deconjugation in AIDS. Gastroenterology 1985; 88: 1455.

Sentongo TA, Rutstein RM, Stettler N et al. Association between steatorrhea, growth, and immunologic status in children with perinatally acquired HIV infection. Arch Pediatr Adolesc Med 2001; 155: 149-153.

  1. Sharpstone DR, Ross HM, Gazzard BG. The metabolic response to opportunistic infections in AIDS. AIDS 1996; 10: 1529-1533.
  2. Laine L, Garcia F, McGilligan K et al. Protein-losing enteropathy and hypoalbuminemia in AIDS. AIDS 1993; 7: 837-840.
  3. Guarino A, Tarallo L, Guandalini S et al. Impaired intestinal function in symptomatic HIV infection. J Pediatr Gastroenterol Nutr 1991; 12: 453-458.
  4. Rollins NC, Filteau SM, Elson I, Tomkins AM. Vitamin A supplementation of South African children with severe diarrhea: optimum timing for improving biochemical and clinical recovery and subsequent vitamin A status. Pediatr Infect Dis J 2000; 19: 284-289.
  5. Gove S. Integrated management of childhood illness by outpatient health workers: technical basis and overview. The WHO Working Group on Guidelines for Integrated Management of the Sick Child. Bull. World Health Organ 1997; 75(Suppl 1): 7-24.
  6. Brink AK, Mahe C, Watera C et al. Diarrhea, CD4 counts and enteric infections in a community-based cohort of HIV-infected adults in Uganda. J Infect 2002; 45: 99-106.
  7. Rollins NC, Pent M, Kindra G et al. CD4 count, HIV viral load and enteric pathogens in HIV-infected children with persistent diarrhea in Durban, South Africa. Pediatric Academic Societies & American Academy of Pediatrics Joint Meeting, Boston, 2000: Poster abstr 1620.
  8. Quesnel A, Moja P, Blanche S et al. Early impairment of gut mucosal immunity in HIV-1-infected children. Clin Exp Immunol 1994; 97: 380-385.
  9. Kotler DP, Gaetz HP, Lange M et al. Enteropathy associated with the acquired immunodeficiency syndrome. Ann Intern Med 1984; 101: 421-428.
  10. Kelly P, Davies SE, Mandanda B et al. Enteropathy in Zambians with HIV related diarrhoea: regression modelling of potential determinants of mucosal damage. Gut 1997; 41: 811-816.
  11. Zeitz M, Ullrich R, Schneider T et al. HIV/SIV enteropathy. Ann NY Acad Sci 1998; 859: 139-148.
  12. Batman PA, Miller AR, Forster SM et al. Jejunal enteropathy associated with human immunodeficiency virus infection: quantitative histology. J Clin Pathol 1989; 42: 275-281.
  13. Wilcox CM, Waites KB, Smith PD. No relationship between gastric pH, small bowel bacterial colonisation, and diarrhoea in HIV-1 infected patients. Gut 1999; 44: 101-105.
  14. Bjarnason I, Sharpstone DR, Francis N et al. Intestinal inflammation, ileal structure and function in HIV. AIDS 1996; 10: 1385-1391.
  15. Delezay O, Yahi N, Tamalet C et al. Direct effect of type 1 human immunodeficiency virus (HIV-1) on intestinal epithelial cell differentiation: relationship to HIV-1 enteropathy. Virology 1997; 238: 231-242.
  16. Kotler DP. Characterization of intestinal disease associated with human immunodeficiency virus infection and response to antiretroviral therapy. J Infect Dis 1999; 179(Suppl 3): S454-S456.
  17. Asmuth DM, Hammer SM, Wanke CA. Physiological effects of HIV infection on human intestinal epithelial cells: an in vitro model for HIV enteropathy. AIDS 1994; 8: 205-211.
  18. Canani RB, Cirillo P, Mallardo G et al. Effects of HIV-1 Tat protein on ion secretion and on cell proliferation in human intestinal epithelial cells. Gastroenterology 2003; 124: 368-376.
  19. Otegbayo JA, Oluwasola AO, Akang EE. Collagenous colitis in an adult patient with chronic diarrhoea: case report. East Afr Med J 2001; 78: 272-274.
  20. Chintu C, Luo C, Baboo S et al. Intestinal parasites in HIV-seropositive Zambian children with diarrhoea. J Trop Pediatr 1995; 41: 149-152.
  21. Powell KR. Guidelines for the care of children and adolescents with HIV infection. Approach to gastrointestinal manifestations in infants and children with HIV infection. J Pediatr 1991; 119: S34-S40.
  22. Yan Z, Nguyen S, Poles M et al. Adenovirus colitis in human immunodeficiency virus infection: an underdiagnosed entity. Am J Surg Pathol 1998; 22: 1101-1016.
  23. Pollok RC. Viruses causing diarrhoea in AIDS. Novartis Found Symp 2001; 238: 276-283.
  24. Orenstein JM, Dieterich DT. The histopathology of 103 consecutive colonoscopy biopsies from 82 symptomatic patients with acquired immunodeficiency syndrome: original and look-back diagnoses. Arch Pathol Lab Med 2001; 125: 1042-1046.
  25. Kelly P, Baboo KS, Wolff M et al. The prevalence and aetiology of persistent diarrhoea in adults in urban Zambia. Acta Trop 1996; 61: 183-190.
  26. Bini EJ, Weinshel EH, Gamagaris Z. Comparison of duodenal with jejunal biopsy and aspirate in chronic human immunodeficiency virus-related diarrhea. Am J Gastroenterol 1998; 93: 1837-1840.
  27. Sewankambo N, Mugerwa RD, Goodgame R et al. Enteropathic AIDS in Uganda. An endoscopic, histological and microbiological study. AIDS 1987; 1: 9-13.
  28. Pavia AT, Long EG, Ryder RW et al. Diarrhea among African children born to human immunodeficiency virus 1-infected mothers: clinical, microbiologic and epidemiologic features. Pediatr Infect Dis J 1992; 11: 996-1003.
  29. Wanachiwanawin D, Chokephaibulkit K, Lertlaituan P et al. Intestinal microsporidiosis in HIV-infected children with diarrhea. Southeast Asian J Trop Med Public Health 2002; 33: 241-245.
  30. Tumwine JK, Kekitiinwa A, Nabukeera N et al. Enterocytozoon bieneusi among children with diarrhea attending Mulago Hospital in Uganda. Am J Trop Med Hyg 2002; 67: 299-303.
  31. Drobniewski F, Kelly P, Carew A et al. Human microsporidiosis in African AIDS patients with chronic diarrhea. J Infect Dis 1995; 171: 515-516.
  32. Enriquez EJ, Avila CR, Santos JI et al. Cryptosporidium infections in Mexican children: clinical, nutritional, enteropathogenic and diagnostic evaluations. Am J Trop Med Hyg 1997; 56: 254-257.
  33. Newman RD, Sears CL, Moore SR et al. Longitudinal study of Cryptosporidium infection in children in northeastern Brazil. J Infect Dis 1999; 180: 167-175.
  34. Cegielski JP, Ortega YR, McKee S et al. Cryptosporidium, enterocytozoon, and cyclospora infections in pediatric and adult patients with diarrhea in Tanzania. Clin Infect Dis 1999; 28: 314-321.
  35. Leav BA, Mackay MR, Anyanwu A et al. Analysis of sequence diversity at the highly polymorphic Cpgp40/15 locus among Cryptosporidium isolates from human immunodeficiency virus-infected children in South Africa. Infect Immun 2002; 70: 3881-3890.
  36. Mayer HB, Wanke CA. Diagnostic strategies in HIV-infected patients with diarrhea. AIDS 1994; 8: 1639-1648.
  37. McGowan I, Hawkins AS, Weller IV. The natural history of cryptosporidial diarrhea in HIV-infected patients. AIDS 1993; 7: 349-354.
  38. Lima AA, Silva TM, Gifoni AM et al. Mucosal injury and disruption of intestinal barrier function in HIV-infected individuals with and without diarrhea and cryptosporidiosis in northeast Brazil. Am J Gastroenterol 1997; 92: 1861-1866.
  39. Guarino A, Castaldo A, Russo S et al. Enteric cryptosporidiosis in pediatric HIV infection. J Pediatr Gastroenterol Nutr 1997; 25: 182-187.
  40. Hicks P, Zwiener RJ, Squires J, Savell V. Azithromycin therapy for Cryptosporidium parvum infection in four children infected with human immunodeficiency virus. J Pediatr 1996; 129: 297-300.
  41. Amadi B, Mwiya M, Musuku J et al. Effect of nitazox-anide on morbidity and mortality in Zambian children with cryptosporidiosis: a randomised controlled trial. Lancet 2002; 360: 1375-1380.
  42. Greenberg PD, Cello JP. Treatment of severe diarrhea caused by Cryptosporidium parvum with oral bovine immunoglobulin concentrate in patients with AIDS. J Acquir Immune Defic Syndr Hum Retrovirol 1996; 13: 348-354.
  43. Schmidt W, Wahnschaffe U, Schafer M et al. Rapid increase of mucosal CD4 T cells followed by clearance of intestinal cryptosporidiosis in an AIDS patient receiving highly active antiretroviral therapy. Gastroenterology 2001; 120: 984-987.
  44. Embree JE, Njenga S, Datta P et al. Risk factors for postnatal mother-child transmission of HIV-1. AIDS 2000; 14: 2535-2541.
  45. Ekpini ER, Wiktor SZ, Satten GA et al. Late postnatal mother-to-child transmission of HIV-1 in Abidjan, Cote d'Ivoire. Lancet 1997; 349: 1054-1059.
  46. Haller JO, Cohen HL. Gastrointestinal manifestations of AIDS in children. Am J Roentgenol 1994; 162: 387-393.
  47. Chandwani S, Kaul A, Bebenroth D et al. Cytomegalovirus infection in human immunodeficiency virus type 1-infected children. Pediatr Infect Dis J 1996; 15: 310-314.
  48. Ukarapol N, Chartapisak W, Lertprasertsuk N et al. Cytomegalovirus-associated manifestations involving the digestive tract in children with human immunodeficiency virus infection. J Pediatr Gastroenterol Nutr 2002; 35: 669-673.
  49. Kitchen BJ, Engler HD, Gill VJ et al. Cytomegalovirus infection in children with human immunodeficiency virus infection. Pediatr Infect Dis J 1997; 16: 358-363.
  50. Kahn E, Greco MA, Daum S. Pathology of the gastrointestinal tract in pediatric AIDS. Surg Pathol 1994; 5: 239-252.
  51. Wilcox CM, Straub RF, Schwartz DA. Cytomegalovirus esophagitis in AIDS: a prospective evaluation of clinical response to ganciclovir therapy, relapse rate, and long-term outcome. Am J Med 1995; 98: 169-176.
  52. Shaik AS, Hadley GP. Surgically significant CMV enterocolitis in children. 25th Biennial Congress of the South African Paediatric Association, and the South African Association of Paediatric Surgeons, 20-24 Oct, 2002 (abstr).
  53. Oshitani H, Kasolo FC, Mpabalwani M et al. Association of rotavirus and human immunodeficiency virus infection in children hospitalized with acute diarrhea, Lusaka, Zambia. J Infect Dis 1994; 169: 897-900.
  54. Cunliffe NA, Gondwe JS, Kirkwood CD et al. Effect of concomitant HIV infection on presentation and outcome of rotavirus gastroenteritis in Malawian children. Lancet 2001; 358: 550-555.
  55. Jere C, Cunliffe NA, Hoffman IF et al. Plasma HIV burden in Malawian children co-infected with rotavirus. AIDS 2001; 15: 1439-1442.
  56. Brasil P, Sodre FC, Cuzzi-Maya T et al. Intestinal microsporidiosis in HIV-positive patients with chronic unexplained diarrhea in Rio de Janeiro, Brazil: diagnosis, clinical presentation and follow-up. Rev Inst Med Trop Sao Paulo 1996; 38: 97-102.
  57. Hautvast JL, Tolboom JJ, Derks TJ et al. Asymptomatic intestinal microsporidiosis in a human immunodeficiency virus-seronegative, immunocompetent Zambian 119 child. Pediatr Infect Dis J 1997; 16: 415-416.
  58. Schmidt W, Schneider T, Heise W et al. Mucosal abnormalities in microsporidiosis. AIDS 1997; 11: 1589-1594.
  59. van den Bergh Weerman MA, van Gool T, Eeftinck 120 Schattenkerk JK, Dingemans KP. Electron microscopy as an essential technique for the identification of parasites in aids patients. Eur J Morphol 1993; 31: 107-110. 121
  60. Spira R, Lepage P, Msellati P et al. Natural history of human immunodeficiency virus type 1 infection in children: a five year prospective study in Rwanda.

Pediatrics 1999; 104: 56. 122

113. Horwood C, Liebeschuetz S, Blaauw D et al. Diagnosis of paediatric HIV infection in a primary health care setting using a clinical algorithm. Bull World Health

Organ 2003; 81: 858-866. 123

114. Coutsoudis A, Bobat RA, Coovadia HM et al. The effects of vitamin A supplementation on the morbidity of children born to HIV-infected women. Am J Public Health

1995; 85: 1076-1081. 124

115. Villamor E, Mbise R, Spiegelman D et al. Vitamin A supplements ameliorate the adverse effect of HIV-1, 125 malaria, and diarrheal infections on child growth.

Pediatrics 2002; 109: E6.

  1. Fawzi WW, Mbise R, Spiegelman D et al. Vitamin A 126 supplements and diarrheal and respiratory tract infections among children in Dar es Salaam, Tanzania. J 127 Pediatr 2000; 137: 660-667.
  2. Bahl R, Bhandari N, Saksena M et al. Efficacy of zinc-fortified oral rehydration solution in 6- to 35-month-old children with acute diarrhea. J Pediatr 2002; 141: 128 677-682.
  3. Bhandari N, Bahl R, Taneja S et al. Substantial reduction in severe diarrheal morbidity by daily zinc supple mentation in young north Indian children. Pediatrics 2002; 109: E86.

Faruque AS, Mahalanabis D, Haque SS et al. Doubleblind, randomized, controlled trial of zinc or vitamin A supplementation in young children with acute diarrhoea. Acta Paediatr 1999; 88: 154-160. Berhane R, Bagenda D, Marum L et al. Growth failure as a prognostic indicator of mortality in pediatric HIV infection. Pediatrics 1997; 100: E7. Arpadi SM, Cuff PA, Kotler DP et al. Growth velocity, fat-free mass and energy intake are inversely related to viral load in HIV-infected children. J Nutr 2000; 130: 2498-2502.

WHO Technical Advisory Group on Nutrition and

HIV/AIDS. Nutrient Requirements for People Living with

HLV/ALDS. Summary report of a Technical Consultation.

Geneva, Switzerland: World Health Organisation, 2003.

O'Keefe EA, Wood R, Van Zyl A, Cariem AK. Human immunodeficiency virus-related abdominal pain in

South Africa. Aetiology, diagnosis and survival. Scand J

Gastroenterol 1998; 33: 212-217.

Borgstein ES, Broadhead RL. Acquired rectovaginal fistula. Arch Dis Child 1994; 71: 165-166.

Oliver MJ. Spontaneously occurring rectovaginal fistu-

lae in children and adults with HIV infection. East &

Central Afr J Surg 1995; 1: 23-25.

Wiersma R. HIV-positive African children with rectal fistulae. J Pediatr Surg 2003; 38: 62-64.

Wang NC, Chang FY, Chou YY et al. Intussusception as the initial manifestation of AIDS associated with primary Kaposi's sarcoma: a case report. J Formos Med

Assoc 2002; 101: 585-587.

Chadwick EG, Connor EJ, Hanson IC et al. Tumors of smooth-muscle origin in HIV-infected children. JAMA 1990; 263: 3182-3184.

Was this article helpful?

0 0
Living Gluten Free

Living Gluten Free

A beginners guide that will reveal how living "G" free can help you lose weight today! This is not a fad diet, or short term weight loss program that sometimes makes you worse off than before you started. This is a necessity for some people and is prescribed to 1 out of every 100 people on earth by doctors and health professionals.

Get My Free Ebook


Post a comment