Special Report

The Threat of Infectious Diseases in Somalia

D. Gray Heppner, Jr., Alan J. Magill, Robert A. Gasser, Jr., and Charles N. Oster

N Engl J Med 1993; 328:1061-1068April 8, 1993

Article

The Four Horsemen of the Apocalypse -- War, Famine, Pestilence, and Death -- ride the arid plains of Somalia. Despite the protection offered by modern chemoprophylaxis, immunization, and preventive medicine, military personnel safeguarding food delivery in Operation Restore Hope are threatened by exotic infectious diseases rarely seen by U.S. physicians. Some require prompt treatment to prevent death (Table 1Table 1Endemic Infectious Diseases of Somalia, with Systemic Presentations.). Many other infections acquired in Somalia will appear soon after exposure, some will become evident after the troops return home, and others will remain latent unless host immunity is compromised. Physicians caring for Somalis, particularly displaced persons in refugee camps, are confronted with a substantial risk of contagion exacerbated by overcrowding, poor sanitation, malnutrition, inadequate immunization, and the absence of rudimentary health care and arthropod-vector control. The ebb and flow of refugees and the long-term absence of comprehensive health reporting require that estimates of the risk of disease be based on isolated studies and historical accounts.

Systemic disorders presenting as acute, life-threatening illnesses include Plasmodium falciparum malaria, epidemic (louse-borne) typhus, meningococcal disease, plague, Congo-Crimean hemorrhagic fever, and relapsing fever. Exposure to rabies must be recognized, and prophylaxis administered to prevent death. Cholera, although not a systemic infection, can cause rapid dehydration and death within 24 hours. Illnesses unlikely to be fatal in the first few days include enteric fever, viral hepatitis, diseases caused by dengue virus and other arboviruses, malaria other than that due to P. falciparum, brucellosis, Q fever, visceral leishmaniasis, murine typhus, African tick typhus, and leptospirosis.

Acute Infections That May Be Rapidly Fatal

Malaria is endemic throughout Somalia. Ironically, in 1854,1,2 44 years before the transmission of malaria by mosquitoes was proved,3 the famed British explorer Sir Richard Burton recorded, but dismissed, the Somali belief that mosquitoes caused malaria. Peak transmission occurs in July and December after semiannual rains; the rates of transmission are higher in the south, with hyperendemic foci along the Shabeelle and Juba river valleys1,4,5. P. falciparum accounts for 95 percent or more of reported cases, P. vivax and P. malariae the remainder5-7. P. falciparum, the most virulent species, is resistant to chloroquine in Somalia both in vitro7-10 and in vivo7,8,10. Forty-three cases of malaria (39 due to P. falciparum and 4 due to P. vivax) had been reported in military personnel as of February 20, 1993 (Lipnick R: personal communication).

Preventing malaria requires aggressive reduction of exposure to night-biting vectors by the use of mosquito nets, insect repellents containing N,N-diethyl-3-methylbenzamide (deet), and permethrin-impregnated clothing; elimination of breeding sites; directed spraying of insecticides; and chemoprophylaxis11. Chemoprophylaxis is best achieved with mefloquine (Lariam, Hoffmann-LaRoche), at a weekly dose of 250 mg. Doxycycline, at a dose of 100 mg daily, is an alternative for aircrew members (mefloquine may interfere with fine motor skills), those taking beta-blockers, and those unable to tolerate mefloquine12-14. Chemoprophylaxis failures are expected as a result of noncompliance, spontaneous resistance,15 or the importation of resistant strains. In addition, prophylaxis with oral primaquine to eliminate persistent hepatic parasites should be given to all patients with confirmed P. vivax, except those who are pregnant and those with a glucose-6-phosphate-dehydrogenase deficiency, and it should be considered for all others on their departure from Somalia14.

Malaria must be excluded in all febrile patients; clinical manifestations vary widely13,16. Exclusion requires serial examination (every 8 hours for 48 hours) of Giemsa-stained blood smears, because infected erythrocytes are periodically sequestered from the peripheral circulation. Uncomplicated cases can be treated with 1000 to 1250 mg of mefloquine given as a single dose or in two divided doses six hours apart or with halofantrine (Halfan, SmithKline Beecham) given in three 500-mg doses six hours apart, and repeated seven days later in non-immune patients14. Three tablets consisting of a combination of 25 mg of pyrimethamine and 500 mg of sulfadoxine (Fansidar, Hoffmann-LaRoche) can be given as a single dose, but treatment failures with this regimen have occurred in neighboring Kenya17. Patients with complicated infections (involving altered mental status, parasitemia of more than 5 percent, hypotension, or end-organ dysfunction) are treated intravenously with quinidine gluconate (a loading dose of 10 to 15 mg per kilogram of body weight in normal saline is given over a four-hour period, followed by a constant infusion of 1.0 to 1.5 mg per kilogram per hour for up to three days)18,19.

Louse-borne typhus, which is due to Rickettsia prowazekii, is a risk for those in contact with refugees20. It presents as a severe, nonspecific febrile illness with chills, myalgias, malaise, and severe headache. On about the fifth day of illness, a macular rash appears on the upper trunk; this becomes maculopapular and then petechial and confluent as it spreads centrifugally, sparing the face, palms, and soles. The mortality rate is decreased by the prompt administration of tetracycline or chloramphenicol21. Murine, or flea-borne, typhus, which is due to R. typhi, causes a similar but milder illness22,23. African tick typhus, caused by R. conorii, is distinguished from louse- or flea-borne typhus by the presence of an eschar at the site of the tick bite and by the rash, which often involves the palms, soles, and face24. A patient with African tick typhus recently presented to the Walter Reed Army Medical Center 10 days after his return from a 3-day visit to Somalia (Williams W: personal communication). The potential impact of this disease is illustrated by a recent outbreak that caused a moderately severe flulike illness in 39 of 169 U.S. troops returning from a two-week deployment to Botswana (Smoak B: personal communication).

Meningococcal disease should pose little threat to soldiers immunized with the quadrivalent (A, C, Y, and W-135) meningococcal vaccine, since the usual African serotype is A or C25. Cases could be caused by other serotypes or occur in persons for whom immunization is not protective26.

Plague was last reported during outbreaks along the Shabeelle River in 1924,1,27 but the existence of competent flea vectors, rodent proliferation, and human migration increase the potential for reemergence of this enzootic disease. Plague most often presents with fever and an intensely painful bubo; pneumonic plague is highly contagious28.

Congo-Crimean hemorrhagic fever is a tick-borne viral disease presenting as hemorrhagic fever with hepatitis. No cases have been reported in Somalia, but the agent is present in ecologically similar areas of neighboring Kenya and Ethiopia29-31. Fulminant disease can occur, with the potential for lethal nosocomial spread. Mortality rates of 40 to 100 percent have been reported in nosocomially infected health care workers32-34. Although the likelihood of an outbreak is low, vigilance must be maintained and strict respiratory and barrier precautions implemented in all suspected cases35. No proved therapy or prophylaxis for Congo-Crimean hemorrhagic fever is available, but ribavirin may be effective for these purposes36,37. Yellow fever has never been reported in Somalia1,38.

Louse-borne (Borrelia recurrentis) and tick-borne (B. duttonii) relapsing fevers due to borrelia spirochetes are characterized by abrupt, severe fever lasting several days, terminating in a crisis with rapid defervescence, severe sweating, and weakness and then, after an interval of several days, recurring one or more times39,40. In louse-borne disease, 5 percent or more of untreated patients may die40. This disease has occurred in Ethiopian refugees in Somalia41. The milder tick-borne relapsing fever, which is endemic in Somalia, typically causes more febrile relapses and has a greater propensity for causing reversible neurologic deficits in non-African patients39,42. The diagnosis is confirmed by identifying spirochetes on a Giemsa- or Wright-stained blood smear. Treatment with a single oral dose of 500 mg of erythromycin, 500 mg of tetracycline, or 100 mg of doxycycline is curative, but is frequently complicated by a severe Jarisch-Herxheimer reaction43,44. These reactions, characterized by rigors, high fevers (temperatures in excess of 40 °C), and severe hypotension, may be fatal45,46. Corticosteroids do not prevent these reactions,43,47 but careful intravenous volume expansion with isotonic fluids is helpful in managing them45,48.

Rabies, endemic in the Horn of Africa, is transmitted by dogs, foxes, and cats, as well as by camels, donkeys, hyenas, badgers, and jackals1,5,27. Clinicians should recognize that rabies can be acquired from saliva across mucous membranes or broken skin and administer prophylaxis to all who might have been so exposed49.

Epidemic cholera broke out in Somalia in 1985,50 but has not been reported in recent years51,52. Severe cholera, as well as infections due to enterotoxigenic Escherichia coli, can present acutely as a rapidly dehydrating diarrhea, leading to death in as few as 24 hours. Primary therapy is the rapid repletion of intravascular volume by the oral or intravenous route53,54. Treatment with antibiotics may shorten the illness and decrease the rate of transmission. Plasmid-mediated resistance to tetracycline, ampicillin, and sulfonamides rapidly emerged and then predominated during the 1985 epidemic, but resistant strains of Vibrio cholerae remained uniformly susceptible to erythromycin50,55.

Other Acute Infections

Other diseases may present acutely, but the need for rapid diagnosis is less urgent. Enteric fever presents with remittent or sustained fever, headache, weakness, and anorexia. Diarrhea or constipation may be present. The disease is diagnosed by isolating Salmonella typhi from blood, urine, or bone marrow56,57. Therapy with ciprofloxacin or ceftriaxone should reduce the mortality rate to less than 1 percent58,59. These medications are preferable to possible alternatives, such as chloramphenicol or ampicillin, because isolates are more likely to be resistant to those antibiotics. The survival of patients with enteric fever and associated shock or altered consciousness is improved by the addition of dexamethasone (3 mg per kilogram every 6 hours for the first 48 hours) to antibiotic regimens60. Intestinal perforation or hemorrhage may occur in untreated patients by the third week of illness.

Hepatitis A,61 hepatitis B,61-64 hepatitis delta,65,66 and hepatitis E67-69 are highly endemic in Somalia, and hepatitis C is present61. Soldiers are protected against hepatitis A by prophylactic immune serum globulin70. Hepatitis B, hepatitis C, and hepatitis delta are usually parenterally or sexually transmitted and should pose a low risk. In contrast, hepatitis E has been responsible for recent outbreaks in Somalia and is a hazard for foreign relief workers67. Immune serum globulin from Western sources is not of prophylactic value, and there is no vaccine for hepatitis E71. The mortality rate is less than 1 percent, except among pregnant women, in which case rates of 17 to 20 percent have been reported68.

Outbreaks of dengue occurred in the 1980s in refugee camps near Hargeysa72 and among foreign workers in Mogadishu73. Classic dengue with fever, chills, sweats, headaches, and back and bone pain is clinically indistinguishable from other endemic arboviral fevers, including sandfly, Rift Valley, West Nile, Sindbis, O'nyong-nyong,74 and chikungunya fevers. Dengue hemorrhagic fever has not been reported in Somalia. Usually, these arboviral fevers present as an acute illness of two to six days' duration after an incubation of two to seven days and may require several weeks of convalescence. Thirty-three cases of dengue fever, one case of Sindbis fever, and one case of West Nile fever had been reported in military personnel in Somalia as of February 20, 1993 (Lipnick R: personal communication).

P. vivax and P. malariae cause a minority of malarial disease in Somalia. These species are expected to be uniformly susceptible to drug therapy. However, mixed infection with P. falciparum and a second species can occur75,76. If there is doubt about the causative agent, the patient should be treated as if P. falciparum is present.

Case reports,1,77 leishmanin skin testing,78 and a serologic survey79 confirm that visceral leishmaniasis is hyperendemic in Somalia. Acute visceral leishmaniasis, frequently mistaken for malaria, can present abruptly with high fever, malaise, cough, and diarrhea80,81. This early syndrome can resolve; progress to classic kala-azar with marked hepatosplenomegaly, pancytopenia, and hyperglobulinemia; or evolve into a chronic viscerotropic form82,83. Diagnosis requires isolation of the parasite from bone marrow, lymph nodes, spleen, or liver. The incubation time is usually months, but incubation periods of 10 years have been reported84. Surprisingly, cutaneous leishmaniasis has not been reported in Somalia, but reports from neighboring countries and the observation of large numbers of people with skin ulcers in Somalia1 make its presence likely.

Seropositivity rates of 37 percent in Mogadishu and 64 percent in the Shabeelle river valley have been reported for leptospirosis85. People in contact with soil or water are at risk. Anicteric leptospirosis may present as aseptic meningitis, gastroenteritis, appendicitis, or undifferentiated fever86,87. Icteric leptospirosis (Weil's disease) may be confused with viral hepatitis, malaria, typhoid fever, or typhus87-89. Diagnosis of this disease in a field laboratory is possible by detection of anti-leptospiral antibodies by IgM-specific dot-enzyme-linked immunosorbent assay90. Doxycycline is effective early in the course of the disease,91 as is intravenous penicillin G in severe disease92.

Gastrointestinal illnesses are more common, though usually less dangerous to the individual patient, than many of the systemic diseases just considered. The spectrum of gastrointestinal pathogens in Mogadishu was evaluated by a study of more than 1600 pediatric outpatients with diarrhea in 1983 and 198493. The authors identified rotavirus in 25 percent, enterotoxigenic E. coli in 11 percent, shigella species in 9 percent, Aeromonas hydrophila in 9 percent, Campylobacter jejuni in 8 percent, V. cholerae non-O 1 in 6 percent, and salmonella species in 4 percent. Giardia lamblia was isolated from 8 percent of these patients, and Entamoeba histolytica trophozoites from 2 percent93. Epidemic shigellosis, with mortality rates estimated at 10 to 15 percent in the local population, has been described94. Antibiotic-susceptibility profiles for Somali isolates of E. coli95 and shigella species96 demonstrated that 50 to 90 percent were resistant to ampicillin, sulfonamides, and tetracycline. Trimethoprim resistance was also described. The E. coli isolates were uniformly susceptible to nalidixic acid95. Given these resistance patterns, fluoroquinolones should be the first choice for empirical antibiotic treatment of diarrhea.

Prevalence surveys of intestinal protozoa found that 2 to 50 percent of examined subjects were infected with Ent. histolytica and 15 to 40 percent were infected with G. lamblia1,97-99. The prevalence of intestinal helminths varies with the population studied. Ascariasis, enterobiasis, trichuriasis, and ancylostomiasis are very common, whereas strongyloidiasis and tapeworm infections are less so5,97-99. Of special concern, given the current concentration of refugees and relief efforts in southern Somalia, is a reported hookworm prevalence approaching 100 percent among agricultural workers along the Juba river valley and a prevalence of 38 to 55 percent in other surveys in southern Somalia. Profound anemia, with hemoglobin levels of 2 to 3 g per deciliter, has commonly complicated hookworm infection in this region1. Thus, ancylostomiasis may be contributing substantially to the high death rates in the region. Hookworm infection may present acutely with midepigastric pain and eosinophilia100.

Sexually transmitted diseases are prevalent101-104. Infection with the human immunodeficiency virus is present, and AIDS has been reported105-107.

Infections with Possible Delayed Presentation

Diseases with prolonged incubation periods are of particular concern to physicians evaluating those who return from Somalia. P. falciparum malaria must be excluded, even if there is no history of a primary attack and the patient received chemoprophylaxis. P. falciparum malaria can present as late as two years after exposure. Hypnozoites of P. vivax can cause disease up to 5 years after exposure in the absence of effective prophylaxis with primaquine, and inadequately treated infections with P. malariae have recurred after 30 years108.

The viral hepatitides may present up to six months after exposure. Convalescence from other viral infections, sandfly fever for example, can be complicated by fatigue, weakness, and depression lasting for months109,110.

Drug-resistant strains of Mycobacterium tuberculosis have not been reported in Somalia, but widespread use of isoniazid in refugee camps and poor compliance suggest that there may be widespread resistance to isoniazid111-113. Therefore, active tuberculosis should be presumed to be resistant to isoniazid, and four-drug therapy with isoniazid, rifampin, ethambutol, and pyrazinamide should be instituted, pending determination of antimicrobial susceptibility114.

Several zoonoses may present after a relief worker has left Somalia. Q fever, endemic in East Africa,115 is highly transmissible, requiring only proximity to a parturient animal or inhalation of dust from an infected herd. Q fever may present acutely as an atypical pneumonia or as an undifferentiated febrile illness. Chronic Q fever can present as culture-negative endocarditis, granulomatous hepatitis, or fever of unknown origin up to seven years after exposure116,117. Brucellosis is acquired by inhalation, the ingestion of milk, or direct contact with animals. Acute brucellosis is nonspecific; chronic infection often causes skeletal, genitourinary, or pulmonary disease118. The disease is diagnosed by isolating the fastidious organism, usually from blood or bone marrow, or by serologic analysis119. Echinococcus granulosus, the agent of hydatid disease, is common in the region1 and presents as a mass lesion years after infection. Exposure to rabies may not be recognized. The disease can occur as long as 12 months after exposure, although this occurs in fewer than 3 percent of cases; hence, this disease remains an unlikely but insidious delayed threat. Patients with delayed rabies may not present with the suggestive prodrome of paresthesias or pruritus at the portal of entry120.

Urinary schistosomiasis caused by Schistosoma haematobium is hyperendemic in the river valleys of southern Somalia, with infection rates of more than 50 percent in many areas5,121-123. Other species have not been described. Acute schistosomiasis, known as Katayama fever, is rarely if ever seen with S. haematobium124. Chronic infection presents months later with terminal hematuria, dysuria, and frequency. The diagnosis should be suspected in persons with a history of exposure to fresh water. The eggs can also be deposited outside the urinary tract and can be responsible for ectopic syndromes125,126. For the optimal detection of S. haematobium eggs, urine should be obtained between 10 a.m. and 3 p.m. If the results are negative, then an examination of stool or a rectal or bladder biopsy may reveal the eggs.

Bancroftian filariasis is known to occur along the adjacent Kenyan coast127. Cahill reported seeing Somalis with elephantoid limbs and scrota who gave a history of repeated attacks of lymphangitis,1 and a serologic survey revealed high rates of seropositivity128. Also common on the Kenyan coast are various animal filariae that have been implicated in human tropical pulmonary eosinophilia129 and obscure neurologic syndromes130. The initial symptoms of filarial infection in nonimmune patients are pain and swelling of the genitalia, arms, or legs associated with headache, backache, nausea, and fatigue131-133. Fever and chills are unusual. The onset is abrupt after an incubation period of 5 to 18 months. Acute lymphadenitis with a retrograde lymphangitis is characteristic. Diagnosis requires isolation of the microfilariae, which are often difficult to find in the early stages of the disease. Because of the nocturnal periodicity of Wuchereria bancrofti microfilariae, a peripheral-blood smear is best obtained around midnight and stained with Giemsa. Concentration methods should be used if no parasites are seen134. Chronic obstructive complications of filariasis require long-term, intense exposure to parasites, but even limited exposure can lead to prolonged symptoms135.

Leprosy can be transmitted by brief contact with patients with multibacillary lepromatous leprosy or by contact with fomites. The incubation period is usually 2 to 5 years, but may be as long as 20 years136. Liver abscess due to Ent. histolytica usually presents without signs of intestinal disease. Serologic analysis is an important aid to diagnosis137,138.

Serologic data139 and the results of histoplasmin skin tests140 suggest that histoplasmosis is common in Somalia, especially in the river valleys. African histoplasmosis, due to Histoplasma capsulatum var. duboisii, probably occurs in addition to disease due to H. capsulatum141,142. African histoplasmosis may present more commonly with focal lesions of the bone and skin as well as with disseminated infection143-146. Prolonged illness and unusual presentations have also been documented147. The yeast form of H. capsulatum var. duboisii in tissue sections is 10 to 15 micrometers in diameter, larger than the yeast form of H. capsulatum, which is 2 to 4 micrometers in diameter148.

Chronic autoinfection with Strongyloides stercoralis, described in World War II and Vietnam veterans, can persist for years and should be considered in cases of recurrent urticaria, abdominal pain, diarrhea, asthma, or eosinophilia149-153. Eosinophilia should also prompt consideration of infection with intestinal helminths, schistosomiasis, and filariasis154.

Latent Infections That Present in Immunocompromised Hosts

Latent infections that can progress to overt disease if host immunity is compromised are of particular concern. Tuberculosis,155 leishmaniasis,156-160 histoplasmosis,161-164 and strongyloidiasis165-168 may emerge years later in association with chemotherapy, organ transplantation, corticosteroid use, AIDS, or intercurrent illness.

Infectious Causes of Mortality in Refugee Camps

Children bear the brunt of famine compounded by disease. The group that is hardest hit are those under five years of age who are living in camps; crude mortality rates (the number of deaths per 10,000 people per day) as high as 69.4 in this group were reported in November 1992 in Baidoa169,170. The stark cumulative effect was revealed in a population-based mortality assessment, which found that 9 percent of the population of Baidoa was less than five years old, as compared with a typical Third World proportion of 20 to 25 percent170. Severe malnutrition, a multitude of endemic diseases, and the virtual absence of medical facilities make attribution of death to a single cause difficult. Nevertheless, surveys of refugee camps identify diarrhea, measles,170 acute respiratory tract infection, and malaria20,169 as the leading infectious causes of death. In recent years, deaths from tuberculosis,111-113 cholera,50 hepatitis E,67 typhus, whooping cough, and relapsing fever have also been reported in refugee camps20.

The susceptibility of refugees to infection is increased by the widespread prevalence of protein-calorie malnutrition, scurvy, iron-deficiency anemia, and vitamin A deficiency20. Infestation with intestinal helminths increases the severity of malnutrition and anemia97-99,171,172. Children in refugee camps are at risk for poliomyelitis, diphtheria, tetanus, pertussis, and measles because of inadequate immunization173,174.

The synergistic toll of malnutrition and infection is well illustrated by the interplay of vitamin A deficiency and measles. Increased catabolism caused by measles increases the vitamin A requirement, yet measles also causes stomatitis, which decreases oral intake, and diarrhea, which decreases the absorption of vitamin A by the gut, thereby exacerbating vitamin A deficiency175. Vitamin A deficiency causes blindness, predisposes patients to respiratory tract infection, and increases mortality. Measles mortality, most often due to supervening bacterial pneumonia, is decreased by the administration of vitamin A supplements176.

Conclusions

The movement of large numbers of soldiers into areas in which they encounter tropical infections has historically presented the clinician with new challenges, such as those presented by the occurrence of hemorrhagic fever with renal syndrome due to hantavirus during the Korean War,177 melioidosis due to Pseudomonas pseudomallei during the Vietnam War,178 and viscerotropic leishmaniasis caused by Leishmania tropica during Operation Desert Storm83. When evaluating a person for an illness temporally related to travel in Somalia, one should keep in mind Pliny the Elder's classic aphorism, “Ex Africa semper aliquid novi” (There is always something new out of Africa).

The opinions or assertions herein are the private views of the authors and are not to be considered as official or as reflecting the views of the Departments of the Army or the Air Force or the Department of Defense.

Source Information

Address reprint requests to Dr. Heppner at the Department of Immunology, Walter Reed Army Institute of Research, Washington, DC 20307-5100.

References

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Citing Articles

1. 1

   Je Rice, SA Skull, C Pearce, N Mulholland, G Davie, JR Carapetis. (2003) Screening for intestinal parasites in recently arrived children from East Africa. Journal of Paediatrics and Child Health 39:6, 456-459
   CrossRef

2. 2

   Kassirer, Jerome P., . (1999) Should Medical Journals Try to Influence Political Debates?. New England Journal of Medicine 340:6, 466-467
   Full Text

3. 3

   Alan J. Magill. (1998) FEVER IN THE RETURNED TRAVELER. Infectious Disease Clinics of North America 12:2, 445-469
   CrossRef

4. 4

   Cabot, Richard C.Scully, Robert E., Mark, Eugene J., McNeely, William F., Ebeling, Sally H., Mankin, H.J.Wu, H.C.. (1996) Case 9-1996. New England Journal of Medicine 334:12, 784-789
   Full Text

5. 5

   Trueman W. Sharp, Robert F. DeFraites, Scott A. Thornton, James P. Burans, Mark R. Wallace. (1995) Illness in Journalists and Relief Workers Involved in International Humanitarian Assistance Efforts in Somalia, 1992–93. Journal of Travel Medicine 2:2, 70-76
   CrossRef

6. 6

   (1993) Infectious Diseases in Somalia. New England Journal of Medicine 329:12, 889-890
   Full Text

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