Personal View

Loa loa—does it deserve to be neglected?

Wolfram Gottfried Metzger, Benjamin Mordmüller

More than 10 million people in western and central Africa are estimated to be infected with Loa loa filarial nematodes. Lancet Infect Dis 2014;
Like most other infectious diseases, L loa filariasis (loiasis) covers a wide range of symptoms. Severe complications 14: 353–57

have been reported; however, most observations are anecdotal, typically in travellers. The widespread use of filaricidal Published Online
December 12, 2013
drugs within eradication programmes of Onchocerca volvulus and Wuchereria bancrofti led to the observation that
http://dx.doi.org/10.1016/
concomitant L loa infection increases the risk of severe treatment-associated, life-threatening complications. S1473-3099(13)70263-9
Initiatives were therefore launched to map the risk of loiasis. Insight about the epidemiology of L loa has advanced Centre de Recherches Médicales
notably; however, its effect on the individual as well as on the community level has not been well studied. In the de Lambaréné (CERMEL),
absence of appropriate studies, L loa is commonly judged a harmless nematode, and loiasis as a separate entity does Lambaréné, Gabon, and
Institute of Tropical Medicine,
not belong to the list of neglected tropical diseases to be controlled or eradicated in worldwide campaigns. We advocate
Eberhard Karls University,
reorientation of research efforts towards a patient-centric view of loiasis and, as a first step, to establish the disease Tübingen, Germany
burden in disability-adjusted life-years of this chronic infection, and to answer the question of whether loiasis should (W G Metzger MD,
be included in future control programmes. B Mordmüller MD)
Correspondence to:
Dr Wolfram Metzger, Institute of
Introduction mutualistic relationship with some filarial nematodes,
Tropical Medicine,
The startling feature of infection with Loa loa filariae is three research groups were looking independently for Wilhelmstrasse 27,
vividly depicted in an early report:1 “…a single woman, the bacteria in L loa worms; none found them.7–9 In other 72074 Tübingen, Germany
aged 29, attended Dr O’Donovan’s clinic at the London studies, awareness of L loa increased as a result of serious wolfram.metzger@uni-
tuebingen.de
Hospital on December 17, 1930. Fifteen months ago she adverse events to ivermectin—especially encephalo-
went to the coastal area of Nigeria as a missionary…on pathies—in patients who were treated for Onchocerca
the boat returning to this country she noticed in a mirror volvulus while co-infected with L loa. Then, a series of
a white worm about one inch long moving in the skin of articles were published on L loa treatment10–21 and
the cheek toward the inner canthus of the left eye. …she epidemiology.22–26 Consequently, the number of
was advised…to apply pressure to prevent the worm from publications on L loa increased substantially in the past
entering the eye, and when she did so the worm retreated 20 years.
and disappeared.” For many years, reports described the
subconjunctival passage of the eye worm through the Epidemiology and diagnosis
patient’s eye (figure 1). Together with the so-called The first comprehensive literature review on L loa
Calabar swelling, this is the visible and pathognomonic epidemiology was published in 1997.27 From 2002 to
symptom of loiasis. Since its first description by a French 2010, a large effort was made to assess L loa prevalence
surgeon located in Santo Domingo in 1770,2 L loa has using large-scale surveys that implemented a short
been a popular topic for case reports of rare diseases. questionnaire for the history of eye worm (rapid
14·4 million people live in high-risk regions, which are assessment procedures for loiasis, RAPLOA). Of the ten
defined as an area where the estimated prevalence of eye countries with endemic L loa, Gabon and Equatorial
worm is greater than 40%, and 15·2 million people live Guinea were classified as high risk, with an estimated
in intermediate risk areas with an estimated prevalence prevalence of eye worm history greater than 40% and
around 30% (20–40%). From these figures, we estimate representing a large proportion of the total high-risk
that at least 10 million people are infected with L loa. The area in Africa; in Gabon, the RAPLOA survey was
endemic countries are: Angola, Cameroon, Central complemented by microscope detection of micro-
African Republic, Chad, Democratic Republic of the filariae, and an overall prevalence of 66% was reported
Congo, Equatorial Guinea, Gabon, Nigeria, Republic of for eyeworm history and 22% for microfilaraemia
Congo, and Sudan.3 In some endemic regions loiasis is (video).28 However, because of their low population, See Online for video
the second or third most common cause of medical these two countries account for less than 5% of the total
consultations.4,5 high-risk population. By contrast, the Democratic
On the basis of our clinical experience in Gabon, we Republic of the Congo (7·4 million) and Cameroon
postulated that L loa might not be as harmless as (4 million) represent 80% of the estimated total
commonly suggested. We searched the literature to population at high risk.3 The epidemiology of this
identify research needs and propose topics that can be parasite is in flux, since the wide distribution of the
addressed by future research programmes. The earliest anthelmintic ivermectin in areas where O volvulus is co-
reference was from the year 1918.6 Many published endemic has led to substantial decreases in the
articles had been written not because loiasis was the abundance of L loa, and high prevalence is found now
main focus of scientific interest, but the attention was mainly in areas that do not harbour O volvulus.
drawn to L loa by other research. For example, when Alongside patient history of an adult worm passing
bacteria of the genus Wolbachia were found to have a through the eye or itchy swellings on the body (Calabar

www.thelancet.com/infection Vol 14 April 2013 353

 Personal View
Carmen L Ospina Salazar, Lambaréné, Gabon
Figure 1: Adult Loa loa filaria decomposing in human eye
This patient was seen by the doctor after an unsuccessful manual extraction
attempt of the worm at home.
Carmen L Ospina Salazar, Lambaréné, Gabon
Figure 2: Loa loa microfilaria in human placenta
Microfilaria in placenta of a young woman.
swellings), an infection with L loa can be diagnosed by the
detection of larvae (microfilariae), which are released by
the adult worms into the peripheral blood. In peripheral
blood samples, microfilariae can be detected with
microscopy and L loa specific DNA with PCR tests. An
additional diagnostic instrument is the detection of L loa
specific antibodies in serum samples. Generally, the
diagnosis of loiasis is challenging for two reasons. First,
densities of microfilariae in the blood are high between
1000 h and 1600 h. Thus, a reliable detection of parasites,
or pathogen-associated molecules, in the peripheral blood
is possible only in the window of a few hours. Second,
more than half of patients harbour adult worms without
detectable microfilariae in the bloodstream at any time.5
These occult carriers are difficult to identify with either
microscopy or highly sensitive and specific PCR.29,30
354
Disease treatment
The WHO-recommended first-line treatment of loiasis is
diethylcarbamazine,31 which has been clinically studied
in patients with onchocerciasis and lymphatic
filariasis.32,33 However, only one randomised controlled
trial has investigated a prophylactic regimen in
immunologically naive volunteers from the US Peace
Corps,34 and we could find no trial on efficacy and adverse
events of diethylcarbamazine treatment in patients from
an endemic region with ongoing loiasis in our literature
search. Effectiveness of diethylcarbamazine has been
seen in expatriate visitors to endemic regions, and several
case reports have been published because patients
suffered adverse events.35–37
Especially in individuals with high burdens of L loa
microfilariae, the use of diethylcarbamazine has
frequently been associated with severe encephalopathy,
not unlike the syndrome evoked by ivermectin in patients
with high microfilaraemia. Unfortunately, strategies to
ameliorate these encephalopathies have not been
identified. In general, patients with high microfilaraemia
bear a high risk for severe side-effects to treatment
brought on by decomposing larvae, and any new therapy
targeting this infection needs to anticipate the possible
consequences. That these reactions typically occur in
remote regions is a serious complication to their
treatment and favourable resolution. Why some of the
patients develop life-threatening treatment complications
and others do not has not been investigated. Diagnostic
methods that can identify people at risk are urgently
needed.
Alternative drugs are ivermectin and albendazole. The
profiles of both drugs are completely different with
respect to L loa. Ivermectin has no activity against adult
worms. It kills microfilariae through an unknown
mechanism that relies on the host’s immune system
(similar to diethylcarbamazine), and can lead to an
overwhelming immune response. As a result, ivermectin
is highly active but not curative (since the adults remain
unaffected) and the safety profile is problematic,
especially in cases of high filarial load where life-
threatening, post-treatment reactions have occurred
repeatedly.17
To extend treatment options, albendazole was studied
in L loa endemic regions.38 Albendazole is effective in
reducing microfilariae through its action on adult worms
and has been useful in treating loiasis refractory to
diethylcarbamazine.39 It does not require a host immune
response. Microfilariae are reduced slowly and the risk to
patients is low compared with diethylcarbamazine and
ivermectin,40 but treatment lasts longer and it does not
sufficiently reduce high microfilarial levels to allow safe
therapy with diethylcarbamazine in most cases.
Both agents, ivermectin and albendazole, have been
investigated by means of randomised controlled trials in
patients infected with L loa.41–45 To improve efficacy and
reduce side-effects, currently proposed therapeutic
www.thelancet.com/infection Vol 14 April 2013

regimens combine these chemotherapeutic agents in
different combinations depending on the microfilarial
load of the patient.46
Another strategy is the physical separation of
microfilariae from the blood by apheresis techniques.
These high-tech methods have been used in a few
patients from resource-rich countries only.47–49 The
treatment of loiasis is therefore difficult because easily
applicable therapies, which can clear parasites and bear a
low risk for side-effects, are not available.
Disease symptoms and burden
The range of loiasis symptoms and complications goes
from no symptoms at all to various severe complications,
such as cerebral (eg, encephalopathy in the absence of
treatment), cardiac (eg, endomyocardial fibrosis),
pulmonary (eg, pulmonary infiltrates), and renal
complications (eg, renal failure), as well as neurological
and psychiatric disorders. Many complications are
presumably due to immune complex deposition and
are frequently accompanied by marked eosinophilia.50,51
Most publications present isolated histories seen in
American or European expatriates and do not focus on
the majority of cases that occur in endemic countries
(figure 2).
Only two studies of residents in endemic areas
exceeded the size of case reports, excluding other
infections and using a control group of non-infected
individuals. One is a cross-sectional study showing that
loiasis (n=142) is associated with pruritus, skin
eruptions, oedemas, joint and muscle pain, and severe
headache, when compared with the non-infected control
group (n=98). As expected, the low number of
participants meant that the risk for severe complications
could not be assessed in this study.52 Uncontrolled
observations in cohorts of African patients confirm
these results.53,54
The other study investigated cardiac complications in
L loa carriers (n=219) versus L loa-negative controls
(n=63). In this study, all three patients with endo-
myocardial fibrosis had detectable L loa infection,
negative stool examination for intestinal helminths, and
marked eosinophilia. However, also in this study, the
number of participants was too low to draw a conclusion
on the cause of this rare complication backed by
statistical significance.55,56
Some studies compare clinical and immunological
parameters in African and expatriate patients. The
findings support the hypothesis that differences in the
modulation of the immune response to parasite
antigens are responsible for much of the variation in
clinical presentation: L loa-naive expatriates developed
more and different symptoms than did endemic
populations.57,58 However, the effect of age on symptoms
and complications of loiasis has not been investigated,
and studies focusing on clinical manifestations in
African infants and children were not found.
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Personal View
Jean Paul Akue, Franceville, Gabon
Figure 3: There is a worm, there are medical records, but is there a disease?
Single sheathed Loa loa larva.
The clinical features of loiasis were the subject of some
doctoral theses in Cameroon.56,59–61 As a big part of the
endemic countries are francophone, the language barrier
might result in an under-representation of French
publications in the scientific arena dominated by English
as lingua franca. This, in consequence, might also
contribute to the low visibility of disease manifestations.62
In general, the roughly 500 PubMed-indexed articles
published within about 100 years is a fairly low number
for an infection affecting more than 10 million people.
The main finding of this literature search is that
systematic studies assessing the overall disease burden
of loiasis do not exist. This finding is noteworthy, because
case reports and medical experience in endemic areas
show that L loa causes a broad range of symptoms and is
a chronic, sometimes lifelong, infection.
One way to measure disease burden is the deter-
mination of disability-adjusted life-years (DALY). The use
of DALYs has become central to quantifying the health
effect of a pathological condition. Certainly, this abstract
indicator is far from perfect, but it shall be useful to
facilitate decisions on the implementation of control
programmes or other health interventions. Oncho-
cerciasis, for example, had directly not caused a single
death, but its global burden was nearly 1 million DALYs
according to the Global Burden of Disease report of 2002;
pruritus caused by onchocercarial filariae accounted for
60% of the DALYs.63
Similar assessments exist for headache caused by
migraine or joint pain caused by rheumatic diseases.
Extensive data analysis has also been accomplished on
other nematodal infections, such as schistosomiasis,
lymphatic filariasis, ascariasis, trichuriasis, and
hookworm disease, on the global and the national level.
355
 Personal View
Search strategy and selection criteria
We searched PubMed, and included all publications with “Loa loa” or “loiasis” in the title.
Non-English publications were included as far as they were indexed in PubMed. Because
some non-English, and some earlier literature, used different spelling, the terms “loaiasis”
and “Filaria loa” were added to the search. References were subjectively labelled by the two
authors in categories: epidemiology, diagnosis, treatment, vector studies, animal models,
host parasite interactions, case reports, “other”, and reviews/comments/editorials. The
rationale behind the chosen labels was to obtain a rough overview of the research done
on L loa. 480 references remained after eliminating double entries in the four lists (last
retrieved Feb 1, 2013). 122 references (25%) were written in 16 languages other than
English, with articles in French representing the biggest part (n=68 [14%]). A third of the
references were case reports (165 of 480 [34%]), and one in ten publications (46 [10%])
were review articles, comments, or editorials. The remaining articles were divided into the
categories of epidemiology (41 [9%]), diagnosis (28 [6%]), treatment (71 [15%]), vector
studies (37 [8%]), animal models (26 [5%]), host parasite interactions (41 [9%]), and
other (25 [5%]).
Conclusions
The chronic nature of infection, range of symptoms and
complications, treatment complications, comorbidity, and
economic restrictions mean that large, standardised, and
longitudinal studies would be needed to assess fully the
effect of L loa on affected populations. Such studies would
be complex and might not be cost-efficient. We suspect
that the paucity of data is evidence that the disease is
viewed as less serious than it really is, and, vice versa—
because the disease is thought to be less serious, no
research efforts are done to determine the disease burden.
As a consequence, research that aims to improve
diagnosis, therapy, and case-management is not funded,
and patients are therefore neglected; loiasis is not listed
as a separate entity in the report on the global burden of
disease.64 Its effect on social life and economy, on the
individual and on the community level, has never been
assessed adequately, and the possible benefits from
disease control, or at the very best, eradication, have
never been estimated (figure 3).
As with many other neglected tropical diseases, loiasis
is a chronic disease of poor populations in resource-
limited countries, which, in turn, can trap these people
in poverty.65 We are well aware that many publications
close with the statement that “more research is needed”.
In the case of L loa infection, this conclusion is
definitively justified. Appropriate primary data for the
disease burden of loiasis (in DALYs) must be gained, and
L loa should be included in research and control
programmes for neglected tropical diseases.
Contributors
Both authors contributed equally to the literature search and writing of
the manuscript.
Conflicts of interest
We declare that we have no conflicts of interest.
Acknowledgments
We thank Marco Jacobi for helping in the literature search and
Sorina Köhler for brushing up our English.
356
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