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Transcript
Review
The new global map of human brucellosis
Georgios Pappas, Photini Papadimitriou, Nikolaos Akritidis, Leonidas Christou, Epameinondas V Tsianos
The epidemiology of human brucellosis, the commonest zoonotic infection worldwide, has drastically changed over
the past decade because of various sanitary, socioeconomic, and political reasons, together with the evolution of
international travel. Several areas traditionally considered to be endemic—eg, France, Israel, and most of Latin
America—have achieved control of the disease. On the other hand, new foci of human brucellosis have emerged,
particularly in central Asia, while the situation in certain countries of the near east (eg, Syria) is rapidly worsening.
Furthermore, the disease is still present, in varying trends, both in European countries and in the USA. Awareness
of this new global map of human brucellosis will allow for proper interventions from international public-health
organisations.
Introduction
USA
Brucellosis is an old disease with minimal mortality. Yet
human brucellosis remains the commonest zoonotic
disease worldwide with more than 500 000 new cases
annually,1–3 is associated with substantial residual
disability,4 and is an important cause of travel-associated
morbidity.5 The global epidemiology of the disease has
drastically evolved over the past decade. We focus on the
current global distribution of the disease and its
relocation during the past decade, and attempt to explain
the rationale behind this evolution and its possible
future projections.
Until the 1960s, most human cases in the USA were
attributed to Brucella abortus, reaching a high of
6321 cases in 1947.27 A massive eradication campaign
resulted in the elimination of cattle brucellosis and a
substantial decline in the incidence of human disease.
During the 1970s brucellosis was mainly attributed to
Brucella suis, prevalent among abattoir workers.28
According to annual reports from the Centers for
Disease Control and Prevention (Atlanta, GA),17
2215 cases were reported in the period 1973–82, and
1201 cases were reported between 1983 and 1992.
1056 cases were reported for the period 1993–2002,
more than half deriving from Texas and California. The
136 cases and incidence of 0·48 cases per million for
2001 represent respective peaks since 1985 and 1983. A
small decline was noted in 2002. Table 2 shows the
average annual incidence per state for 1993–2002, and
figure 2 depicts the incidence distribution per state.
Global status
Figure 1 depicts the incidence of human brucellosis
worldwide. Table 1 shows the countries with the highest
annual incidence of human brucellosis from 2000
onwards, as well as the incidence for selected other
countries.
Lancet Infect Dis 2006; 6: 91–99
GP, LC and EVT are at the First
Division of Internal Medicine of
the Medical School at the
University of Ioannina, Greece;
PP is at the Pediatrics
Department of the University
Hospital of Ioannina, Greece; and
NK is at the Internal Medicine
Department of the General
Hospital “G Hatzikosta”,
Ioannina, Greece.
Correspondence to:
Dr Georgios Pappas, Internal
Medicine Department, University
Hospital of Ioannina, 45110,
Greece. Tel: +30 26510 49453;
[email protected]
Annual incidence of brucellosis
per 1000 000 population
500
50–500 cases
10–50
2–10
2
Possibily endemic, no data
Non-endemic/no data
Figure 1: Worldwide incidence of human brucellosis
http://infection.thelancet.com Vol 6 February 2006
91
Review
Country and reference
Incidence (annual cases per
million of population)
Europe
Albania6
Bosnia and Herzegovina7
Denmark7
France7
Former Yugoslav Republic of Macedonia8
Georgia7
Germany7
Greece9
Ireland7
Italy10
Netherlands7
Norway7
Portugal11
Russia7
Serbia and Montenegro7
Spain12
Sweden7
Switzerland13
UK14
63·6
20·8
0·7
0·5
148
27·6
0·3
20·9
1·3
9
0·5
0·7
13·9
4·1
8·4
15·1
0·3
1·5
0·3
Africa
Algeria8
Cameroon7
Egypt15
Eritrea16
Ethiopia7
Mali8
Namibia8
Tunisia7
Uganda7
84·3
Endemic, no specific data available
2·95
5·48
Endemic, no specific data available
2
4·9
35·4
0·9
North America
Canada7
USA17
Mexico18
0·09
0·4
28·7
Central and South America
Argentina8
Chile7
Colombia7
Guatemala16
Panama7
Peru7
8·4
0·6
1·85
15·7
10·1
34·9
(continues)
(continued)
Asia
Afghanistan7
Armenia16
Azerbaijan8
China19
India
Iraq7
Iran8
Israel7
Jordan20
Kazakhstan21
Korea, South7
Kuwait7
Kyrgyzstan16
Lebanon22
Mongolia23
Oman7
Pakistan
Saudi Arabia24
Syria7
Tajikistan7
Turkey7
Turkmenistan7
United Arab Emirates25
Uzbekistan7
Oceania
Australia26
3·8
31·3
52·6
8
No data available, possibly endemic
278·4
238·6
9·2
23·4
115·8
1
33·9
362·2
49·5
605·9
35·6
No data available, possibly endemic
214·4
1603·4
211·9
262·2
51·5
41
18
0·9
Table 1: Global incidence of human brucellosis
the actual picture of brucellosis in the USA today is
represented: a disease caused by B melitensis, affecting
the Hispanic population, and localised in areas
neighbouring Mexico.29,30 A recent report from San
Diego, California showed a limited area where B abortus
is prevalent.31 The disease is imported through the
US/Mexican border by means of infected dairy products,
particularly Mexican soft cheese.32–34 The increased
incidence in Illinois remains of obscure aetiology.
Latin America
Most of the US cases are attributed to Brucella
melitensis. 647 (79·4%) of the 815 patients for whom
ethnicity was documented were of Hispanic origin.
During 1993–2002, 46 states reported at least one case,
and 26 states reported at least one case in 2002. Illinois,
Florida, Texas, Arizona, Colorado, and California
reported at least one case annually, while Maine,
Vermont, Rhode Island, North Dakota, West Virginia,
and Nevada reported no cases at all. The annual
incidence is highest in Wyoming, although the small
number of cases precludes evaluation of the clinical
importance of this incidence. The average incidence is
increased in North Carolina and Arkansas due to
clusters of 27 cases in 1993 and nine cases in 2001,
respectively. Most cases in northern states probably
represent imported disease acquired through
international travel or infected food preparations
imported from endemic areas. This is not the case for
west south central, mountain, and Pacific states, where
92
Mexico remains one of the most important reservoirs of
human brucellosis. Data from the Mexican Ministry of
Health’s epidemiology directorate18 for the years
1996–2003 show a decline until 2000, and a subsequent
increase in the annual number of cases reported; 3008
cases were reported in 2003. Whether this increase is
actual or related to improvements in notification
systems35 cannot be determined. The disease is localised
in two zones: the northern districts neighbouring the
USA—eg, Coahuila, Nuevo Leon, Sonora, and
Chihuahua (average annual incidence 186, 85, 57, and
54 cases per million respectively)—and northwestern
and west central districts—eg, Sinaloa, Zacatecas,
Durango, and Guanajuato (although the latter district
exhibits a continuous incidence decline). The most
important parameter of the epidemiology of human
brucellosis in Mexico is the effect the endemicity of the
northern districts exhibits on the epidemiology of the
disease in the USA. Even strict border control cannot
http://infection.thelancet.com Vol 6 February 2006
Review
contain a zoonosis; thus eradication cannot be achieved
by means of national control programmes, especially in
areas where immigration is common. A global, or at
least continental plan has to be undertaken to ensure
eradication.
Animal brucellosis exists throughout Central
America36 but human disease is not endemic. Guatemala
and Panama are exceptions, according to annual data
from the World Organisation for Animal Health (OIE).7,8
South America has been traditionally considered an
endemic area of human brucellosis, B melitensis being
prevalent in Peru and west Argentina, and B abortus in
east Argentina37,38 and other South American countries.
Data from the OIE imply that brucellosis is still
important in Peru and Argentina.8 There are no data
available for Brazil, which hosts the largest commercial
cattle population in the world, and is presumably at risk
of increased prevalence of human B abortus disease.
Under-reporting may be an obstacle in evaluating the
true incidence in Brazil39 and neighbouring countries:
brucellosis is not included in the notifiable diseases for
which surveillance is active (even in Peru). With the
exception of Peru and Argentina, South America should
be excluded from the highly endemic global zones of
human brucellosis.
European Union/western Europe
Brucellosis-free status has been granted by the European
Union (EU) to Sweden, Denmark, Finland, Germany,
the UK (excluding Northern Ireland), Austria,
Netherlands, Belgium, and Luxembourg.40 Norway and
Switzerland are also considered brucellosis-free
countries. Most of these countries do report a small
number of cases annually, mainly in travellers to
endemic countries or immigrants from endemic
areas.41,42 A B abortus epidemic has been evolving since
1998 in Northern Ireland, with 89 cases in total. Reemergence of human brucellosis does not seem possible
in western Europe, especially since adequate
surveillance systems exist. Eradication campaigns in
southern European member countries will probably
prevent trafficking of the disease inside the EU.
The Mediterranean basin is an acknowledged endemic
region of human brucellosis. The disease was initially
described in Malta, where sporadic cases are noted
nowadays.
France is an example of successful eradication. More
than 800 cases of human brucellosis were reported in
1976, declining to 405 cases in 1983, 125 cases in 1990,
and 44 cases in 2000.43 According to OIE data for the
following years, the annual number of cases reported
remained low.7 Most of these cases are due to localised
outbreaks in southern provinces, and are related to the
consumption of dairy products imported from Spain.
The evolution of eradication is also represented in
regional distribution. Corsica reported most of the
national cases during 1990–95, yet no cases were
http://infection.thelancet.com Vol 6 February 2006
Area
New England
Maine
New Hampshire
Vermont
Massachusetts
Rhode Island
Connecticut
Mid-Atlantic
New York
New Jersey
Pennsylvania
East north central
Ohio
Indiana
Illinois
Michigan
Wisconsin
West north central
Minnesota
Iowa
Missouri
North Dakota
South Dakota
Nebraska
Kansas
South Atlantic
Delaware
Maryland
DC
Virginia
West Virginia
North Carolina
South Carolina
Georgia
Florida
East south central
Kentucky
Tennessee
Alabama
Mississippi
West south central
Arkansas
Louisiana
Oklahoma
Texas
Mountain
Montana
Idaho
Wyoming
Colorado
New Mexico
Arizona
Utah
Nevada
Pacific
Washington
Oregon
California
Alaska
Hawaii
Total
Number of
cases
11
0
1
0
8
0
2
27
13
3
11
111
12
1
68
24
6
52
9
22
15
0
1
2
3
126
2
5
1
6
0
46
3
18
45
23
4
7
7
5
310
24
8
5
273
91
1
5
7
18
12
43
5
0
305
10
8
272
2
13
1056
Annual incidence
(cases per million)*
0·08
0
0·08
0
0·13
0
0·06
0·07
0·07
0·04
0·09
0·25
0·11
0·02
0·57
0·24
0·11
0·28
0·19
0·77
0·27
0
0·13
0·12
0·11
0·26
0·27
0·1
0·19
0·09
0
0·61
0·08
0·23
0·3
0·14
0·1
0·13
0·16
0·18
1·03
0·95
0·18
0·15
1·38
0·54
0·11
0·41
1·46
0·45
0·69
0·92
0·24
0
0·7
0·17
0·24
0·83
0·33
1·09
0·39
*Average incidence for 1993–2002, derived from the annual summaries of notifiable
disease of the Centers for Disease Control and Prevention.18 1998 population used in
estimating incidence, as provided in the same source.
Table 2: Reported cases and annual incidence of brucellosis in the USA,
1994–2003
93
Review
Annual incidence of brucellosis
per 1000 000 population
1
0·5–1
0·1–0·5
0·1
No cases
Figure 2: Brucellosis incidence in the USA, 1993–2002
reported in the past 3 years. Small foci still exist in the
southeastern provinces of Savoie and Alpes Maritimes.
Although massive progress has been achieved in
minimising human disease in Spain, the country still has
one of the highest annual incidences in Europe. Data are
available for 1997–2003 from the National Centre of
Epidemiology.12 A substantial, consistent decline in
annual number of cases is evident, reaching an all-time
low of 642 cases in 2003. This decline is reflected in most
autonomous communities. However, the annual
incidence remains high in Andalusia, Castille-La Mancha,
Aragon, and Castille-Leon (70, 68, 60, and 56 cases per
million per year, respectively). The highest annual
incidence is noted in Extremadura, but the situation in
this region has been improving substantially throughout
this period. Although the consistent decline in the
incidence of human brucellosis in Spain underlines the
systematic national approach towards disease control,
Spain remains an endemic area. However, one can be
confident that the situation will change, approaching the
French situation, in the years to come.
Portugal has achieved pronounced progress in
minimising human brucellosis. Data from the
Portuguese Ministry of Health11 for 1999–2003 indicate a
steep decline in annual incidence, from 70 cases per
million in 1999 to less than 14 cases per million in 2003.
The progress is attributed to enhanced control in certain
endemic northern and central districts. However, the
situation has not improved substantially in southern
regions—eg, the district of Alentejo, where the annual
incidence remains high. This district neighbours the
endemic region of Extremadura in Spain; as already
discussed, the situation in Extremadura has improved in
recent years, and it will be interesting to observe the
dynamics of human disease trafficking, and particularly
whether persistence of the disease in the Portuguese
region will induce a resurgence in the Spanish region.
94
In Italy, a unique pattern in the epidemiology of
human brucellosis has been observed between 1994
and 2003, according to data derived from the Italian
Ministry of Health.10 A steady decline in the number of
annual cases has been consistently observed over the
past 30 years: in 1976, 3318 cases were reported in
total, and by 1986 the annual number of cases dropped
below 2000. A gradual, although inconsistent, decline
was subsequently observed. However, the annual
incidence of the disease has not dropped in a uniform
fashion across the country: of the 520 cases reported in
2003, 488 (93·2%) were reported from four southern
regions, compared with 63·7% in 1994. Sicily alone
reported 57·6% of the 2003 cases. The average annual
incidence for Sicily, Calabria, Puglia, and Campania
was 111, 48, 44, and 37 cases per million, respectively.
None of the northern and central regions reported
more than ten cases in 2003, and these cannot be
attributed to local epidemiological factors. In Italy,
human brucellosis has travelled to the south,
something explained by socioeconomic factors; the
schism of Italy to the rich north and the poor south is
nowhere more pronounced than in the incidence of
human brucellosis.
Greece remains in the list of the 25 countries with the
highest incidence worldwide. The annual incidence,
according to data from the Centre for Special Infections
Control9 is gradually declining. Concern exists that these
data may not represent the actual situation: the data is
generally inconsistent—eg, in 1995 only six cases were
officially reported. Under-reporting is also evident in the
regional distribution of cases, since the annual number
of cases reported for the northwestern region of Epirus
represents a gross underestimation according to our
personal experience and a recent epidemiological study
in this area.44 One reason for poor reporting, apart from
inadequate awareness from private sector practitioners,
http://infection.thelancet.com Vol 6 February 2006
Review
is that a percentage of new cases consists of patients
living in southern Albania, who commonly seek medical
advice in Greece. These patients are reported neither in
Greece nor in Albania. Even with official estimates, the
annual incidence in Epirus is high—over 70 cases per
million per year. Various parameters account for the
increased incidence in this region: illegal trafficking of
herds or even dairy products through the
Greek/Albanian border, inadequate implementation of
control programmes,45 poor health literacy of both
general population and medical practitioners, fear of
economic losses through slaughtering of infected
livestock
belonging
to
patients
undergoing
epidemiological surveillance, and most importantly, the
overall socioeconomic status of the area. A measure of
the relation between brucellosis endemicity and
socioeconomic status can be drawn from the gross
domestic product (GDP) for certain endemic regions of
the EU, such as Epirus. Figure 3 shows the GDP values
of various EU regions: the endemic areas of Portugal
and Greece are characteristically the poorest areas of the
EU. The disease is also widespread on the Greek
mainland, with the average annual incidence for
Thessaly, northern Greece, and Peloponissos
approaching 120, 51, and 48 cases per million,
respectively. Figure 4 depicts the brucellosis free and
endemic regions of western and southern Europe.
The Balkan peninsula
Apart from Greece, two other countries in the Balkan
peninsula have the highest disease incidence in Europe.
In the Former Yugoslav Republic of Macedonia, human
brucellosis is almost an epidemic, although the annual
incidence is gradually decreasing.8 The incidence is also
high in Albania,6 where a substantial degree of under100
Incidence
80
Brucellosis status
Endemic
Brucellosis free
Non-endemic
Figure 4: Brucellosis status in Europe
reporting exists due to inadequate health networks and
patient migration to Greece. The effect such an endemic
site exerts on neighbouring countries has been already
discussed, but is further underlined by a recent increase
in the reported cases from Bosnia-Herzegovina,7 and in
the region of Kosovo, where, according to the data from
OIE,7 the annual incidence for 2004 approached 20 cases
per million.
60
Eastern Europe
40
20
0
40·0
60·0
80·0
100·0
120·0
140·0
GDP
Figure 3: Gross domestic product and endemicity of brucellosis for EU
regions and countries
Gross domestic product (GDP) according to official EU data.46 Data as follows (in
parentheses, endemicity in annual cases per million of population and GDP as
the percentage of median EU GDP before the expansion, respectively). Greece:
Thessaly (87·5/60·2), Epirus (31·4/54), northern Greece (24·6/65·2). Italy: Sicily
(60·4/65·3), Calabria (19·9/62·1), Campania (15·6/65·1), Puglia (14·7/65),
Piemonte (1·4/115·1), Lombardia (0·9/131·3), Toscana (0·6/111·1), Emilia
Romana (0·5/126·2), Veneto (0·2/115·8). Portugal: Alentejo (56·2/56·9),
central (27·5/56·9), north (8·4/56·9), Lisbon and Vale do Tejo (4·7/94·7). Spain:
Extremadura (54·1/53·5), Castille-La Mancha (51·6/67·1), Andalusia
(32·5/63·1), Castille-Leon (31/78), Catalonia (7·7/100·7), Madrid (5·2/112·4),
Basque country (1·4/105·1). Denmark: (2·6/115·3). Germany: (0·3/100·4).
France: (0·5/104·8). Ireland: (1·3/117·6). Sweden (0·3/106·1). UK: (0·3/105·4).
http://infection.thelancet.com Vol 6 February 2006
Brucellosis is not endemic in eastern Europe.
Characteristically in Poland, the disease is limited to
veterinarians or is imported from Mediterranean
countries.47 Brucellosis in Russia nowadays is mainly a
disease of the Caucasian districts—eg, Dagestan, where
the annual incidence exceeds 100 cases per million of
population48—and districts neighbouring republics of
the former Soviet Union with a high incidence of
brucellosis. However, substantial under-reporting may
also exist.
Asia
The middle east has traditionally been considered as an
endemic area. Indeed, five of the ten countries with the
highest incidence for human brucellosis are in this
area.
95
Review
Syria has the highest annual incidence worldwide,
reaching an alarming 1603 cases per million per year
according to data from OIE.7 The annual cases reported
are practically doubling each year, although this may be
attributed to enhanced surveillance.
An increase in the annual number of cases reported
has been also observed in Turkey, exceeding
15 000 cases in 2004.7 Brucellosis is particularly
endemic in the poor eastern regions. Numerous reports
have addressed the epidemiology of the disease in
isolated areas from this region,49 although a coordinated
national approach is still missing. The relation of poor
socioeconomic status and brucellosis incidence, as
outlined in the EU, probably applies here too:
numerous studies focusing on seroprevalence,
summarised by Cetinkaya and colleagues,50 show that
the proximity of a region either to Europe or to Ankara
is accompanied by lower seroprevalence rates, possibly
due to enhanced application of the Turkish Brucellosis
Challenge Project that has been running for the past 20
years.50
The situation in Iran is improving, according to data
from the National Commission on Communicable
Diseases Control. In 1989 the annual incidence exceeded
1000 cases per million;51 in 2003, the annual incidence
had fallen to 238·6 cases per million.8 Still, human
brucellosis remains a huge burden for this country.
Data from OIE were recently made available for the
incidence of human brucellosis in Iraq,7 underlining the
huge endemicity of the disease in this region, despite
ongoing attempts to control both animal and human
disease.52,53 Whether control can be achieved in a state
still plagued by war and famine is questionable;
moreover, the endemicity of the disease in this area may
raise concerns, since a purely endemic brucellosis case
in an international soldier stationed in Iraq might cause
alarm of a possible biowarfare incident. Similarly, the
endemicity of the disease in Afghanistan cannot be
disputed, although substantial data are lacking. The first
official report from the OIE from the region, in 2004,7
with an estimated incidence of 3·8 cases per million of
population, might be a gross underestimation of the
actual incidence.
Brucellosis is endemic in the southern region of
Oman, with an annual incidence exceeding 1000 cases
per million.7
Saudi Arabia is also a vast reservoir of human
brucellosis. Regional endemicity varies in Saudi Arabia,
partly according to climate factors: a rainy season in an
area would result in increased grass growth and thus
influx of shepherds and flocks.54 The increased
incidence of brucellosis in this country is also attributed
to massive importations of uncontrolled slaughter
animals and inadequate quarantine procedures.55 The
absence of health literacy, which could interrupt the
direct link between animal and human disease, is also
critical.56
96
In the United Arab Emirates, most cases are reported
from Dubai,25 a popular international travel destination,
underlining the importance of the disease in the field of
travel medicine.
Kuwait is a prime example of modification of the
epidemiology of human brucellosis by political factors:
20 years ago, the annual incidence exceeded 500 cases per
million, mainly due to widespread animal brucellosis.51
Massive loss of livestock during the 1991 Iraqi invasion
resulted in a substantial decrease in human cases in the
following years; however, this decrease was not sustained
over time,7 and the region is still endemic.
In Jordan, the estimated incidence of human
brucellosis exceeded 300 annual cases per million in the
recent past.57 Data from the Ministry of Health denotes
ongoing control of the disease between 1996 and 2003.20
Similar control has been achieved in Israel, a country
that can no longer be considered endemic.7 However, an
increased number of cases reported by Palestine in
recent years58 could endanger the continuing decline of
brucellosis prevalence in Israel.
Endemicity of the disease in Lebanon has been steady
over the past 10 years, especially in the Beqaa region,
according to data from the Ministry of Public Health.22
One distinct characteristic of the disease in this country
is that the most cases are noted in female patients, by
contrast with the rest of the world, possibly reflecting an
increased transmission as a foodborne disease (via milk
consumption) or increased participation of women in
procedures associated with brucellosis transmission (eg,
milking).
Seven republics of the former Soviet Union are
included in the 25 countries with the highest incidence
of the disease worldwide, while another country of this
region, Mongolia, is ranked second. The situation in
central and western Asia is dramatic: in Kyrgyzstan,
control of brucellosis has become a national priority,
since the already extremely high prevalence may
actually be tripling: more cases were reported in the
first half of 2003 than in the whole of 2002.59 In
Tajikistan and Kazakhstan the annual cases reported
are rapidly increasing, according to OIE data, when
compared with WHO data from 1993–98.60 A rapid
increase can be observed in Mongolia according to data
from the National Statistic Office for the period up to
2000.23 Data from the Ministry of Health of Azerbaijan
for the years up to 2000 show that the annual incidence
is declining.61 Data from OIE7,16 show a steady incidence
pattern for Armenia, Georgia, Uzbekistan, and
Turkmenistan.
These countries have emerged as the most important
loci of human brucellosis worldwide in recent years, and
the seemingly uncontrollable, constantly increasing
incidence poses a serious public-health problem,
especially in the context of inadequately developed
health-care networks. Moreover, since a substantial
percentage of the population in these countries relies on
http://infection.thelancet.com Vol 6 February 2006
Review
livestock for their survival, the disease affects the
economic stability of these countries.
How did these new foci of brucellosis emerge? All of
these countries were part of the former Soviet Union, or
were Eastern bloc satellite states. The evolution from a
socialist state to free market economy resulted in the
loss of strict livestock control. Furthermore, the
transition of the health system during this period
precluded early recognition of the disease, or
intervention for the emerging trends in human beings
and animals.62 Economic instability precludes further
planning of such interventions, even if proven cost
effective.63 However, it is possible that the endemic was
already underway, but under-reporting took place
before political transition. Either way, central policy
directly influenced the natural history of human
brucellosis in these areas, and international
intervention is urgently needed. Interest and financial
and scientific support from international organisations
could be of huge benefit for these countries, but has not
yet emerged.
Most data available about the prevalence of
brucellosis in China are derived from the work of Deqiu
and colleagues.64 A massive vaccination programme of
the human population at risk of acquiring brucellosis
took place between 1964 and 1976. The annual number
of cases reported exhibited a gradual decline, reaching
an all-time low of almost 500 cases in 1994. Thereafter
annual number of cases increased, approaching
1500–3000, without a reciprocal increase in the
prevalence of animal brucellosis. This discrepancy may
be attributed to increased awareness and enhanced
laboratory diagnosis; however, others propose a relation
with climate factors such as the periodicity of the El
Niño phenomenon.64 A steep increase in the reported
cases of human brucellosis was noted during the first
half of 2004, with cases for this period reaching 5753,
according to the Chinese Ministry of Health.19
B melitensis is the commonest pathogen isolated,
although B abortus and B suis prevail in certain
provinces
(Sichuan
and
Guangxi/Guangdong,
respectively). The geographic distribution has also
evolved, with the disease travelling south. Until 1980
the incidence was highest in the provinces of Inner
Mongolia, Jilin, and Helongiiang, in northeastern
China. However, in the past 15 years the prevalence is
highest in the eastern central provinces of Shanxi,
Hebei, and Henan. Tibet remains a region with
increased endemicity.
According to data from OIE,7 an increasing number of
human cases of brucellosis has been noted during
2003–04 in South Korea, the aetiology and significance
of which remains obscure.
The disease is endemic in India, with numerous
reports of cases from isolated areas in the literature,65
and an acknowledged prevalence of animal brucellosis,66
but official data of the incidence of human disease are
http://infection.thelancet.com Vol 6 February 2006
lacking. Animal disease exists also in Pakistan, but there
are no data for the incidence of human disease.
Australia
A limited number of cases of human brucellosis are
reported annually from Australia, according to the
National Notifiable Diseases Surveillance System,26
almost exclusively from the area of Queensland, one of
the poorest areas of the country.
Africa
North Africa has been traditionally considered endemic
for brucellosis. Data on the prevalence of the disease in
Egypt are scarce, with reports from national authorities
probably underestimating the true prevalence of the
disease, since they are derived from selected medical
institutions.16 There are also no official data for Morocco;
the
disease
may
be
endemic
along
the
Moroccan/Algerian border. Limited data exist about
Libya, while the incidence in Tunisia may be an
underestimate of the actual situation.7 Algeria has the
tenth highest annual incidence worldwide,8 but the
annual number of cases reported remained steady
during the last decade. Various WHO programmes have
focused on controlling brucellosis in these countries,51
although available data would support the urgent need
for such intervention only for Algeria and Tunisia.
Brucellosis exists throughout sub-Saharan Africa, but
essentially nothing is known about its prevalence. Most
African countries are of poor socioeconomic status, with
people living with and by their livestock, while health
networks and surveillance and vaccination programmes
are virtually non-existent. Moreover, there are far more
morbid endemic infectious diseases, particularly
malaria. Most febrile patients in these countries are
initially empirically diagnosed as suffering from
malaria, and only a small part of non-responders may be
further tested for brucellosis. Most of the data are
derived from small seroepidemiological studies of
patients with fever or high-risk populations.67 According
to data from OIE for 2004,7 Cameroon, Ethiopia, Kenya,
Nigeria, Tanzania, and Uganda reported the existence of
human cases of brucellosis, while in 2003 similar
reports8 existed for Burkina Faso, Republic of Congo,
Eritrea, Mali, Namibia, and Swaziland. Ghana, Togo,
and Chad are probably also endemic according to
seroepidemiological studies.67,68
Brucellosis cannot be considered an emergency for
Africa since there are other, more morbid, infectious
priorities. Moreover, control of animal disease might
incorporate the slaughtering of infected animals (since
mass vaccination campaigns demand funds and
adequate health-care networks), further compromising
the socioeconomic status of the susceptible population;
in Africa, one can assume, it is better to live with
brucellosis than try to eradicate it and then starve to
death.
97
Review
Search strategy and selection criteria
Data on the prevalence of human brucellosis for each country
from 1990 onwards were sought from health ministries or
other official national organisations, public-health
international organisations, and the medical literature.
Medical literature was searched through Medline (but also
general search engines), using “brucella” or “brucellosis” and
individual country and region names as keywords. PROMEDmail was also used, searching with the keywords “brucellosis”
and individual country names. When available, official
national data were used, even if not in concordance with data
from international organisations. For countries without such
official data, data from international organisations were used.
Medical literature was used only when including
epidemiological information, or (in the case of
seroprevalence studies) in the absence of any other data
regarding disease status in a country. Serial data on incidence
were evaluated for the presence of epidemiological trends
correlating with sanitary, socioeconomic, and political
characteristics of individual countries. In calculating the
annual incidence, when this information was not provided in
the source references, population data derived from official
publications such as the CIA World Factbook71 were used.
Conclusions
The traditional perception of human brucellosis, as
reproduced in most reviews of the disease,69,70 is of a
zoonotic disease prevalent in countries of the
Mediterranean basin, the near east, South America, and
possibly sub-Saharan Africa. Yet, in the past 15 years, the
epidemiology of human brucellosis has evolved,
reflecting alterations in socioeconomic parameters,
improvements in recognition and notification systems,
outcomes of ongoing eradication programmes of animal
brucellosis, and the evolution of the “global village”
through international tourism. New endemic foci have
emerged, warranting eradication programmes that
escape national boundaries. Financial and scientific
support from international organisations should target
the new endemic areas and become a global health
priority. Enhanced surveillance of human brucellosis
may be responsible for the alteration in the endemicity
of the disease in certain countries, but this fact serves
only to underline the magnitude of the problem and the
possibility of it further inflating in the near future. The
fact that the continuing existence of human (and animal)
brucellosis extends beyond medical and veterinary
duties and encompasses political factors goes to show
that the eradication of the disease will not be an easy task
for the future.
Conflicts of interest
We declare that we have no conflicts of interest.
References
1
Corbel MJ. Brucellosis: an overview. Emerg Infect Dis 1997; 3:
213–21.
98
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
Joint FAO/WHO expert committee on brucellosis. World Health
Organ Tech Rep Ser 1986; 740: 1–132.
Pappas G, Akritidis N, Bosilkovski M, Tsianos E. Brucellosis.
N Engl J Med 2005; 352: 2325–36.
Solera J, Lozano E, Martinez-Alfaro E, Espinosa A, Castillejos ML,
Abad L. Brucellar spondylitis: review of 35 cases and literature
survey. Clin Infect Dis 1999; 29: 1440–49.
Memish ZA, Balkhy HH. Brucellosis and international travel.
J Travel Med 2004; 11: 49–55.
World Organisation for Animal Health. Handistatus II: zoonoses
(human cases): global cases of brucellosis in 2000. http://www.oie.
int/hs2/gi_zoon_mald.asp?c_cont=6&c_mald=172&annee=2000
(accessed Dec 13, 2005).
World Organisation for Animal Health. Handistatus II: zoonoses
(human cases): global cases of brucellosis in 2004. http://www.oie.
int/hs2/gi_zoon_mald.asp?c_cont=6&c_mald=172&annee=2004
(accessed Dec 13, 2005).
World Organisation for Animal Health. Handistatus II: zoonoses
(human cases): global cases of brucellosis in 2003. http://www.oie.
int/hs2/gi_zoon_mald.asp?c_cont=6&c_mald=172&annee=2003
(accessed Dec 13, 2005).
Centre for Special Infections Control. Annual reported cases of
notifiable diseases. http://www.keel.org.gr/stanalysis (accessed
Aug 1, 2005).
Ministry of Health, Italy. Results of epidemiological research.
http://www.ministerosalute.it/promozione/malattie/datidefcons.
jsp (accessed Dec 13, 2005).
Ministry of Health, Portugal. Doenças de Declaração Obrigatória,
1999-2003. http://www.dgsaude.pt/upload/membro.id/ficheiros/
i007192.pdf (accessed Dec 13, 2005).
National Centre of Epidemiology, Spain. Obligatory notifiable
diseases, 2003. http://cne.isciii.es/htdocs/ve/Edo2003.htm
(accessed Dec 13, 2005).
Swiss Federal Office of Public Health. Reports of infectious
diseases. http://www.bag.admin.ch/infreporting/mv/e/index.htm
(accessed Dec 13, 2005).
UK Department for Environment Food and Rural Affairs. UK
zoonoses reports. http://www.defra.gov.uk/animalh/diseases/
zoonoses/reports.htm (accessed Dec 13, 2005).
Ministry of Health and Population, Egypt. Enhanced surveillance
for communicable diseases. http://www.geis.fhp.osd.mil/GEIS/
Training/EgyptSurv2000.htm (accessed Dec 13, 2005).
World Organisation for Animal Health. Handistatus II: zoonoses
(human cases): global cases of brucellosis in 2002. http://www.oie.
int/hs2/gi_zoon_mald.asp?c_cont=6&c_mald=172&annee=2002
(accessed Dec 13, 2005).
Centers for Disease Control and Prevention. Summary of notifiable
diseases, United States, 2003. http://www.cdc.gov/mmwr/sum
mary.html (accessed Dec 13, 2005).
Ministry of Health, Mexico. Epidemiological information. http://
www.dgepi.salud.gob.mx/infoepi/index.htm (accessed Dec 13, 2005)
Xinhua News Agency. Health ministry increases efforts to contain
brucellosis. http://service.china.org.cn/link/wcm/Show_Text?info_
id=115313&p_qry=brucellosis (accessed Dec 13, 2005)
Ministry of Health, Jordan. Annual statistical report: notifiable
communicable diseases. http://db-server.moh.gov.jo:7777/servlets/
svr_pack.Incidsrve (accessed Nov 24, 2005).
White N. Kazakhstan in a fight against brucellosis. Casper-Star
Tribune http://www.1wyo.net/KAZAKHSTAN/introduction.html
(accessed Dec 14, 2005)
Lebanese Ministry of Public Health, Epidemiology Surveillance
Unit. http://www.public-health.gov.lb/esu/LEBANON.shtml
(accessed Jan 3, 2006).
Ebright JR, Altantsetseg T, Oyungerel R. Emerging infectious
diseases in Mongolia. Emerg Infect Dis 2003; 9: 1509–15.
World Organisation for Animal Health. Handistatus II: zoonoses
(human cases): global cases of brucellosis 1998. http://www.oie.
int/hs2/gi_zoon_mald.asp?c_cont=6&c_mald=172&annee=1998
(accessed Dec 14, 2005).
United Arab Emirates Ministry of Health. Brucellosis distribution
of reported cases by Medical District UAE 1994-2000. http://www.
moh.gov.ae/moh_site/prev_med/anbk/statistics/comdis/zoono/
stat6/t1.htm (accessed Dec 14, 2005).
http://infection.thelancet.com Vol 6 February 2006
Review
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
Australian Department of Health and Aging. National notifiable
diseases system. http://www9.health.gov.au/cda/Source/Rpt_4_sel.
cfm (accessed Dec 14, 2005).
Wise RI. Brucellosis in the United States. Past, present, and future.
JAMA 1980; 244: 2318–22.
Buchanan TM, Hendricks SL, Patton CM, Feldman RA. Brucellosis
in the United States, 1960–1972; An abattoir-associated disease.
Part III. Epidemiology and evidence for acquired immunity.
Medicine (Baltimore) 1974; 53: 427–39.
Doyle TJ, Bryan RT. Infectious disease morbidity in the US region
bordering Mexico, 1990–1998. J Infect Dis 2000; 182: 1503–10.
Fosgate GT, Carpenter TE, Chomel BB, Case JT, DeBess EE,
Reilly KF. Time-space clustering of human brucellosis, California,
1973–1992. Emerg Infect Dis 2002; 8: 672–78.
Troy SB, Rickman LS, Davis, CE. Brucellosis in San Diego:
epidemiology and species-related differences in acute clinical
presentations. Medicine (Baltimore) 2005; 84: 174–87.
Young EJ, Suvannoparrat U. Brucellosis outbreak attributed to
ingestion of unpasteurized goat cheese. Arch Intern Med 1975; 135:
240–43.
Thapar MK, Young EJ. Urban outbreak of goat cheese brucellosis.
Pediatr Infect Dis 1986; 5: 640–43.
Taylor JP, Perdue JN. The changing epidemiology of human
brucellosis in Texas, 1977–1986. Am J Epidemiol 1989; 130:
160–65.
Luna-Martinez JE, Mejia-Teran C. Brucellosis in Mexico: current
status and trends. Vet Microbiol 2002; 90: 19–30.
Moreno E. Brucellosis in Central America. Vet Microbiol 2002; 90:
31–38.
Trujillo IZ, Zavala AN, Caceres JG, Miranda CQ. Brucellosis.
Infect Dis Clin North Am 1994; 8: 225–41.
Samartino LE. Brucellosis in Argentina. Vet Microbiol 2002; 90:
71–80.
Poester FP, Goncalves VS, Lage AP. Brucellosis in Brazil.
Vet Microbiol 2002; 90: 55–62.
European Commission. Report on trends and sources of zoonotic
agents in the European Union and Norway, 2003. Brucella. http://
europa.eu.int/comm/food/food/biosafety/salmonella/02_brucella_
2003.pdf (accessed Dec 14, 2005).
Eriksen N, Lemming L, Hojlyng N, Bruun B. Brucellosis in
immigrants in Denmark. Scand J Infect Dis 2002; 34: 540–42.
Al Dahouk S, Nockler K, Hensel A, et al. Human brucellosis in a
nonendemic country: a report from Germany, 2002 and 2003.
Eur J Clin Microbiol Infect Dis 2005; 24: 450–56.
Institut de Veille Sanitaire, France. Brucellose. http://www.invs.
sante.fr/surveillance/brucellose/default.htm (accessed Dec 24,
2005).
Avdikou I, Maipa V, Alamanos Y. Epidemiology of human
brucellosis in a defined area of northwestern Greece.
Epidemiol Infect 2005; 133: 905–10.
Godfroid J, Kasbohrer A. Brucellosis in the European Union and
Norway at the turn of the twenty-first century. Vet Microbiol 2002;
90: 135–45.
European Commission. Third report on economic and social
cohesion. http://europa.eu.int/comm/regional_policy/sources/
docoffic/official/reports/cohesion3/cohesion3_en.htm (accessed
Dec 14, 2005).
Czerwinski M. Human brucellosis in Poland. Przegl Epidemiol
2005; 59: 323–25 (in Polish).
Isaev AN, Omarieva EIa, Liamkin GA. Epidemiologic situation of
brucellosis in the regions of the Republic of Dagestan affected by
the flood of 2002. Zh Mikrobiol Epidemiol Immunobiol 2003; 6
(suppl): S78–81 (in Russian).
Aygen B, Doganay M, Sumerkan B, Yildiz O, Kayabas U. Clinical
manifestations, complications, and treatment of brucellosis: a
retrospective evaluation of 480 patients. Med Malad Infect 2002; 32:
485–93.
http://infection.thelancet.com Vol 6 February 2006
50
51
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67
68
69
70
71
Cetinkaya F, Nacar M, Koc AN, Gokahmetoglou S, Aydin T.
Prevalence of brucellosis in the rural area of Kayseri, Central
Anatolia, Turkey. Turk J Med Sci 2005; 35: 121–26.
Regional Animal Disease Surveillance and Control Network, Food
and Agriculture Organization of the United Nations. A perspective
of brucellosis surveillance in North Africa and Middle East.
http://www.fao.org/WAICENT/FaoInfo/Agricult/AGA/AGAH/ID/
Radiscon/brucactsurv.pdf (accessed Dec 14, 2005).
United States Agency for International Development. Iraq
reconstruction and humanitarian relief weekly update number 34
(FY 2004). http://www.reliefweb.int/rw/rwb.nsf/
AllDocsByUNID/442ddae9e2c8c46a85256ea900679403 (accessed
Jan 3, 2006).
UN Office for the Coordination of Humanitarian Affairs. Iraq: new
campaign to control brucellosis. http://www.irinnews.org/
report.asp?ReportID=47021&SelectRegion=Middle_East&SelectCo
untry=IRAQ (accessed Dec 14, 2005).
Elbeltagy KE. An epidemiological profile of brucellosis in Tabuk
Province, Saudi Arabia. East Mediterr Health J 2001; 7: 791–98.
Memish Z. Brucellosis control in Saudi Arabia: prospects and
challenges. J Chemother 2001; 13 (suppl): S11–17.
Bilal NE, Jamjoom GA, Bobo RA, Aly OF, el-Nashar NM. A study
of the knowledge, attitude and practice (KAP) of a Saudi Arabian
community towards the problem of brucellosis. J Egypt Public
Health Assoc 1991; 66: 227–38.
Issa H, Jamal M. Brucellosis in children in south Jordan. East
Mediterr Health J 1999; 5: 895–902.
Husseini AS, Ramlawi AM. Brucellosis in the West Bank,
Palestine. Saudi Med J 2004; 25: 1640–43.
UN Office for the Coordination of Humantiarian Affairs.
Kyrgyzstan: focus on brucellosis in south. http://www.irinnews.
org/report.asp?ReportID=37604&SelectRegion=Central_Asia
(accessed Dec 14, 2005).
WHO. Country reports: 8th report of the WHO surveillance
programme for control of foodborne infections and intoxications in
Europe, 1999–2000. http://www.who.int/foodsafety/publications/
foodborne_disease/dec2003/en (accessed Dec 14, 2005).
Azerbaijan Republic, Ministry of Health. Infectious diseases (total).
http://www.mednet.az (accessed Oct 3, 2005).
Manaseki S. Mongolia: a health system in transition. BMJ 1993;
307: 1609–11.
Roth F, Zinsstag J, Orkhon D, et al. Human health benefits from
livestock vaccination for brucellosis: case study. Bull World Health
Organ 2003; 81: 867–76.
Deqiu S, Donglou X, Jiming Y. Epidemiology and control of
brucellosis in China. Vet Microbiol 2002; 90: 165–82.
Thakur SD, Thapliyal DC. Seroprevalence of brucellosis in man.
J Commun Dis 2002; 34: 106–09.
Renukaradhya GJ, Isloor S, Rajasekhar M. Epidemiology, zoonotic
aspects, vaccination and control/eradication of brucellosis in India.
Vet Microbiol 2002; 90: 183–95.
McDermott JJ, Arimi SM. Brucellosis in sub-Saharan Africa:
epidemiology, control and impact. Vet Microbiol 2002; 90: 111–34.
Schelling E, Diguimbaye C, Daoud S, et al. Brucellosis and Q-fever
seroprevalences of nomadic pastoralists and their livestock in
Chad. Prev Vet Med 2003; 61: 279–93.
Araj GF. Human brucellosis: a classical infectious disease with
persistent diagnostic challenges. Clin Lab Sci 1999; 12: 207–12.
Young EJ. An overview of human brucellosis. Clin Infect Dis 1995;
21: 283–89.
Central Intelligence Agency. The world factbook.
http://www.cia.gov/cia/publications/factbook/index.html (accessed
Dec 13, 2005).
99