Coxiella burnetii in Dromedary Camels (Camelus dromedarius): A Possible Threat for Humans and Livestock in North Africa and the Near and Middle East?

Abstract

The "One Health" concept recognizes that human health is connected to animal health and to the ecosystems. Coxiella burnetii-induced human Q fever is one of the most widespread neglected zoonosis. The main animal reservoirs responsible for C. burnetii transmission to humans are domesticated ruminants, primarily goats, sheep, and cattle. Although studies are still too sparse to draw definitive conclusions, the most recent C. burnetii serosurvey studies conducted in herds and farms in Africa, North Africa, Arabian Peninsula, and Asia highlighted that seroprevalence was strikingly higher in dromedary camels (Camelus dromedarius) than in other ruminants. The C. burnetii seroprevalence in camel herds can reach more than 60% in Egypt, Saudi Arabia, and Sudan, and 70 to 80% in Algeria and Chad, respectively. The highest seroprevalence was in female camels with a previous history of abortion. Moreover, C. burnetii infection was reported in ticks of the Hyalomma dromedarii and Hyalomma impeltatum species collected on camels. Even if dromedary camels represent <3% of the domesticated ruminants in the countries of the Mediterranean basin Southern coast, these animals play a major socioeconomic role for millions of people who live in the arid zones of Africa, Middle East, and Asia. In Chad and Somalia, camels account for about 7 and 21% of domesticated ruminants, respectively. To meet the growing consumers demand of camel meat and milk (>5 million tons/year of both raw and pasteurized milk according to the Food and Agriculture Organization) sustained by a rapid increase of population (growth rate: 2.26-3.76 per year in North Africa), dromedary camel breeding tends to increase from the Maghreb to the Arabic countries. Because of possible long-term persistence of C. burnetii in camel hump adipocytes, this pathogen could represent a threat for herds and breeding farms and ultimately for public health. Because this review highlights a hyperendemia of C. burnetii in dromedary camels, a proper screening of herds and breeding farms for C. burnetii is urgently needed in countries where camel breeding is on the rise. Moreover, the risk of C. burnetii transmission from camel to human should be further evaluated.

Keywords: Coxiella burnetii; dromedary camel (Camelus dromedarius); epidemiology; human—animal coexistence; zoonoses awareness.

Figure 1

Schematic representation of human Q fever epidemiology around the world. With the exception of Antarctica and New Zealand, Q fever is a global zoonosis present in North America, South America, Europe, Asia, Africa, and Australia/Oceania. The clinical manifestation of Q fever in human is usually an undifferentiated febrile illness. Q fever was described for the first time in humans in 1937 by Burnet, who investigated several cases of Australian abattoir workers suffering from undifferentiated febrile illness (15, 16). During the Second World War (1941–1944), the Q fever disease was reported among German soldiers stationed in the Balkans, Southern Italy, Corsica, in English and American allied troops in Central Italy, and soldiers in Crimea and Ukraine. That is why the disease has had many synonyms: Olympus fever, Crimean fever, flu Balkan flu, Cretan pneumonia, Euboea fever, fever of the 7 days, or Derrick and Burnet's disease (17). The causative agent of the disease first identified by Cox in the United States, and formerly named Rickettsia diasporica, was definitively renamed Coxiella burnetii (–20). The figure illustrates the history of the major human epidemics of Q fever (outbreaks >10 linked cases) from 1950 (when the Third World Health Assembly passed a resolution calling for study of the prevalence of Q fever throughout the world) to the present day. Although C. burnetii infection has been classified as a notifiable animal disease by the World Organization for Animal Health, OIE (14), the lack of mandatory reporting of human Q fever cases in most countries, the predominance of asymptomatic forms, the clinical polymorphism, and the difficulty of diagnosis are likely to lead to a significant underestimation of the true incidence of the disease in humans. In Europe where the ECDC carries out a regular epidemiological surveillance, only 1,023 of 4,245 Q fever cases confirmed during the 2013–2017 period were reported by the European countries (21). It is impossible to evaluate the number of cases for the Asian and African continents. ND, not determined.

Figure 2

Schematic representation of human Q fever around the Mediterranean. Left panel: map of the Mediterranean basin. The Mediterranean Sea is bordered by 22 riparian countries. The countries of the Northern Mediterranean coast are represented in dark blue, and the countries of the Southern Mediterranean coast are represented in tanned brown. Right panel: confirmed human Q fever cases per country during the period 2013 to 2017 according to the ECDC (21). Q fever surveillance report, 2017. Values between brackets indicate the average number of Q fever cases per 100,000 inhabitants per year over the 5 years period. Regarding Italy, no data were available for the years 2013, 2014, and 2015. The number of cases of Q fever for Israel over the period 2013 to 2017 was extrapolated from the data published by Yarrow and colleagues (111). ND, not determined. Human Q fever occurs mostly in the form of sporadic cases. Sometimes outbreaks of Q fever were reported in humans. The main epidemics of Q fever described during the last 40 years in people living on the Northern coast of the Mediterranean basin are as follows: 2003 (60 cases), 2004 (16 cases), 2014 (50 cases) in Spain; 1992 (40 cases), 1996 (204 cases), 2002 (126 cases), 2009 (50 cases), 2014 (46 cases) in France; 1993 (58 cases), 2003 (133 cases) in Italy; 2007 (33 cases) in Slovenia; 2004 (14 cases) in Croatia; 2007 (42 cases) in Albania; 2009 (58 cases) in Greece; and 2002 (19 cases) in Turkey. Human Q fever outbreaks are poorly documented concerning the countries of the Southern Mediterranean Sea coast. An epidemics of Q fever was described in 1955 in Algeria with 175 cases.

Figure 3

Priority diseases of camelids according to OIE (240). A list of diseases affecting camels and that appear to be priorities for the OIE to improve diagnostic capacity and establish guidelines for trade of camels and camel products was drawn up in 2014 by the OIE ad hoc Group on camel diseases. These experts divided the priority diseases into three groups: (1) significant diseases; (2) diseases for which camelids are potential pathogen carriers; (3) minor or non-significant diseases. Regarding the priority viral diseases (significant diseases), only camelpox and rabies were listed [foot and mouth disease (FMD) that concerns bactrian camels only, also belonged to the list]. The ad hoc Group classified MERS-CoV, Rift valley fever, and orbivirus-induced diseases (BT, AHS, EHD) among the diseases for which camelids are potential pathogen carriers (the bovine viral diarrhea that concerns the New World camelids also belonged to that list). Regarding bacteria, the ad hoc Group classified brucellosis, tuberculosis, paratuberculosis, anthrax, caseous lymphadenitis, and pasteurellosis in the significant diseases category. Trypanosomosis was classified in the significant parasitic diseases of camelids. It should be noted that coxiellosis is not mentioned in the lists of priority camel diseases for the World Organization for Animal Health, OIE. However, C. burnetii has been classified as a notifiable animal disease by this international office (14).

Figure 4

Schematic representation of animal reservoirs diversity and main routes of animal-to-human transmission of Q fever. Up to now, domestic ruminants were considered the principal reservoirs for C. burnetii and were frequently incriminated as sources of Q fever outbreaks in humans. However, in North Africa and Middle East were camels live, it was reported that most of the time the seroprevalence of anti–C. burnetii Ig was much higher in dromedary camels than in other ruminants. C. burnetii shedding is higher in vaginal mucus and feces than in milk. The infection in humans by Coxiella burnetii is mainly by inhalation of aerosols. It was evidenced that C. burnetii can be transmitted during arthropod blood-sucking. Among ticks, the Hyalomma dromedarii that colonize dromedari camels was found infected with C. burnetii. Human populations at risk of C. burnetii infection are pastoral communities, farmers, slaughterhouses workers, tanneries workers, veterinarians, or individuals handling infected livestock, especially animals giving birth. Raw milk drinkers are also at risk. With the increasing demand of milk and camel meat in urban areas, there is a potential threat for millions of people.

Figure 5

Schematic representation of Camelidae evolution, migration, and domestication. The earliest known Camelidae, named Protylopus and Poebrotherium, appeared roughly 40 million years ago in the North American. During the transition from the Eocene to the Oligocene geological period (about 34 million years ago), the climate in North America is expected to have changed for cooler and drier, and Camelidae began to genetically diverge (407). This was supported by the discovery of the fossil of Paracamelus in Canada in 1913 where this ancestor of Camelus bactrianus and Camelus dromedarius was expected to have inhabited there about 3.5 million years ago when a warmer climate allowed forests to spread near the Arctic Circle (408). About 6 to 8 million years ago, Camelini gradually moved across the land that connected North America to Asia (this land bridge appeared some 8 million years ago, and it remained practicable until it was submerged about 14,500 years ago). According to Wu et al. (409), during the species evolution, they diverged into (i) large Camelidae (Camelini), which lived in North America and next moved westward across the land that connected North America with Asia, then Middle East and North Africa; and (ii) small Camelidae (Lamini), which dispersed South (currently South America). Subsequently about 5 to 8 million years ago, Camelini further evolved into Camelus, which include two species: Camelus bactrianus (the two-humped camel; weight: 600–1,000 kg; size 1.6–1.8 m) and Camelus dromedarius (the single-humped camel; weight: 400–600 kg; size 1.6–2.0 m). Lamini subdivided into two genera: Lama and Vicugna. The earliest evidence for the dromedary domestication is dated about 3,000 years ago near Abu Dhabi on the Arabian Gulf. Northern Arabian tribes began to use dromedary camels as riding animals (410). Dromedary camels were progressively domesticated in North Africa. Gift of camels was a source of camel spread around the Mediterranean. Currently, there are 33 million of domestic Camelus dromedarius living in semiarid and arid regions of Africa and the Middle East, 3 million of domestic Camelus bactrianus that live from the cold steppes of Central Asia to the border of Manchuria in China, and a small population (1,000 camels) of Camelus ferus, the Wild Bactrian, which survives in the Northwest China and the Gobi Desert of Mongolia (Camelus ferus diverged from Camelus bactrianus about 0.7 million years ago) (411). Dromedary camels from India were also introduced in central Australia. Females are only able to conceive from 3 years old and can live up to 30 to 40 years old.

Figure 6

Schematic representation of dromedary camel distribution in the world. The Arabic generic term commonly used for camel is “ibl.” Male camel between 6 and 20 years old are named “jamal” (also the Arabic word for beauty). Currently, there are ~33 million dromedary camels (or humpback camels) worldwide, with highest numbers (77%) in Africa and the Middle East. The geographical location of the dromedary is in the belt of the tropical and subtropical dry zones of Africa, but its presence extends to Western Asia and Northwest India (blue area on the map). Dromedary camels are found in 35 native countries ranging from Senegal to India and from Kenya to Turkey. The number on the map show the population of dromedary camels in each country in 2017 expressed in thousands of “tropical livestock units” (TLUs), according to FAO (369). For example, the largest dromedary camel populations are found in Chad (7,285,309 camel heads) and Somalia (7,222,081 camel heads), followed by Sudan (4,849,003 camel heads) and Kenya (3,338,757 camel heads). Regarding the countries of the Southern coast of the Mediterranean Sea, the current livestock situation is as follows: 59,000 camels for Morocco; 381,882 camels for Algeria; 237,005 camels for Tunisia; 64,469 camels for Libya; 149,224 camels for Egypt; 5,530 camels for Israel; 66,390 camels for Syria; and 14,322 camels for Jordania. A massive dromedary camel (300,000 now-feral dromedary camels) implantation was made in the last century in Australia from camels imported from India (not shown); very specific introductions were also made in the United States, Central America, South Africa, and Europe; they are indicated by blue stars (437). Another member of the Camelidae family, the Camelus bactrianus (or two-humped camels) with a distinguished geographical distribution is present from the cold deserts of Central Asia to the border of Manchuria in China (see Figure 3). Both C. bactrianus and Camelus dromedary species can cohabit in a few places such as western Asia.

Figure 7

Suggested flowchart to monitor farms against the risk of C. burnetii infection. This logigram takes into account the surveillance, the alert, and the measures to be taken in case of presence of C. burnetii–infected animals in a herd. With regard to the specific actions to be implemented, they relate to both general safety measures and specific measures for sick camels or herds with sick animals and farmers.