A review of the regulatory texts on rabies published between 1913 and 2014 in Moroccan official journal¹ is realized with focus on the legal status of rabies. The key points of each text are presented and general evolution of legislation related to rabies is discussed.

Epidemiological data concerning animal and human rabies cases were collected from published bibliographical references and epidemiological reports issued by the competent public authorities, and more especially those of Morocco’s National Food Safety Office (ONSSA) for animal rabies cases and the Ministry of Health for human cases. In the event of contradictory data from different sources, the highest figure has been chosen due to the substantial risk of underreporting (13). The epidemiological characteristics of animal rabies in Morocco are discussed for the period from 1928 to 2015. There follows a presentation and discussion of the rabies patterns in Morocco (reservoir, animal species affected, seasonal changes, and geographical distribution) as well as measures taken at different times to tackle the disease and the suggestions of various authors in order to improve the situation. Mapping of the evolution of the number of animal rabies cases in the Moroccan provinces was performed using ArcGIS 10.1 software. The number of human rabies cases reported annually from 1974 to 2015 is analyzed and discussed. There is a discussion on the geographical distribution of cases of human rabies. The provided PEP protocol is discussed as well as the laboratory diagnosis. Propositions of improvement are formulated. A review of the genetic characterization of rabies virus isolates in Morocco is realized. Molecular epidemiology data are compared with classical epidemiology findings.

Different NRCPs are presented. The achievements and deficiencies of plans are presented and the causes of their limited success analyzed.

It is crucial to remain informed about the dog population in order to draw up a realistic and effective canine rabies control plan. A synthesis of the studies that are interested in the size of the Moroccan canine population is carried out in order to have an estimate of this population. This is based on a comparison between the results of estimations of the dog population in the framework of an amendment to the 1993 rabies control plan, the NRCP of 2001–2010 and other international studies or studies in Maghreb countries. The data are extrapolated depending on the human:dog ratio chosen in order to estimate the size of the dog population. Demographic data were provided by official Moroccan authorities (Health Ministry website: http://www.sante.gov.ma). The current state of dog population control and suggestions for improvement are also presented.

The vaccination coverage of the dog population is estimated by combining data on vaccination in urban areas by private veterinarians with that in rural areas following government-run mass vaccination campaigns. Dog population data are related to the estimated human:dog ratio. Vaccination coverage is analyzed and suggestions put forward on how to improve the situation. Data on vaccination in urban areas were extrapolated from the number of doses of rabies vaccine sold between 2009 and 2015 to veterinarians in the private sector. The data were obtained from veterinary pharmaceutical companies with a rabies vaccine registered in Morocco² during the same period. Propositions for dog population vaccination coverage amelioration are formulated with reference to Moroccan experiments in oral dog rabies vaccination.

The “One World, One Health” concept is highlighted by international organizations such as FAO, OIE, and WHO as the most efficient way of controlling zoonotic diseases. The actions taken in Morocco are assessed in the light of this concept, examples, and suggestions given.

Morocco has a wealth of regulations on animal rabies control with a new text every 9 years. These regulations were first focused in people treatment after rabies exposition on IPT (14) and at antirabies institute of Marie-Feuillet hospital in Rabat (15). The measures were also concentrated on prevention of exposure to rabid animals either imported (16) or locally by instigating measures (17) to control stray dogs in both urban settings (18) and the countryside (19). Parenteral vaccination of dogs was already mandatory in 1928 (20) early and quickly after OIE 1927 conference on rabies and mandatory antirabies vaccination of cats was instaured on 1934 (21).

This basic regulatory framework has been updated in several occasions either within mandatory notifiable animal diseases list update in 1977 (22) or by updating specific measures to control rabies in 2000, 2005, and 2014 (23–25).

This regulation evolves from the vizirial orders in 1915, 1927, 1928, 1934, 1936, to decrees in 2000, 2005, and 2014, which have more regulatory weight.

The regulations cover mandatory rabies vaccination of dogs and measures to be taken in the event of contamination but they do not cover management of the dog population or the concept and actions of “responsible dog ownership”. The latter concept implies registering and identifying dogs, preventing their negative impact on society and controlling breeding. The legislation should also cover mass control actions for stray dogs (means of capture and humane euthanasia) in accordance with OIE rules on animal welfare (26).

It should be noted that national regulations are not fully applied. The mandatory vaccination of dogs is not monitored and there are no legal sanctions should a dog be found to be unvaccinated (25).

The first rabies vaccination was performed in Morocco in 1911 by a rabies vaccine for human and veterinary use produced at IPT (1, 27). Since that, exposed people were treated and from 1923 to 1932 a total of 361 people received PEP in IPT (21). The number of exposed treated people increased to reach an average of 1,500 person per year between 1951 and 1958 (28).

Veterinary authority started dogs preventive antirabies vaccination in 1928 and an average of 671 dogs per year were vaccinated between 1928 and 1933 (27, 29). This number increased to reach 10,000 dogs per year between 1945 and 1965 (30).

An average of 302 (minimum 68 and maximum 663) animal rabies cases was registered between 1942 and 1968 (28, 31–33) demonstrating an active animal rabies surveillance system based on Casablanca laboratory.

Table 1 summarizes the data relating to the 1971 to 2015 period concerning animal rabies, the number of dogs vaccinated and culled, the number of human cases, and the number of people given PEP. We can identify an increasing trend of animal rabies cases number up to 1982 from where this trend decreases. This can be visualized in Figure 1, which traces evolution of animal rabies cases, number of vaccinated and culled dogs from 1942 to 2015. The animal rabies cases number follows a distribution with an ascending phase in which the number of animal rabies cases increases and a descending phase from 1982. The year 1982 coincides with start of WHO rabies fight in Maghreb zone (3). Those efforts led to first NRCP (1986–1990) launch. Figure 1 shows also that the number of vaccinated dogs per year increases considerably in the beginning of the control plan rising from 2,730 dogs in 1982 to 25,000 dogs in 1983 and 229,231 dogs in 1989. This figure then dwindled before increasing once again during the amended rabies control plan of 1994, reaching 325,780 dogs. Similarly, a peak of 450,917 dogs vaccinated was reached in 2005 under the 2001–2010 rabies control program. This evolution in the number of vaccinated dogs in peaks during the maximal activity of different rabies control plans is characteristic. The decrease in the number of vaccinated dogs is thought to be linked to the veterinary services efforts to control other livestock diseases (Figure 1) (5, 34).

Up to 1992, the number of dogs culled was always greater than the number of dogs vaccinated. Since 1992, the culling of dogs has been stopped in the context of rabies control but is still practiced to limit the problem of stray dogs in urban environments (Figure 1).

Several studies have investigated the epidemiological status of rabies in Morocco. We selected the nine that we considered most relevant and which cover the period (1928–2015) (2, 6, 28, 29, 33, 35, 37, 56, 57). Several of the epidemiological characteristics of rabies in Morocco appear stable over the studied period (1928–2015).

Since 1980s, several different NRCPs have followed in succession: –

NRCP covering 1986–1990: plan drawn up as part of the WHO rabies control program in Maghreb countries (3, 4). An interministerial committee was set up to draft a NRCP, whose broad lines included:

Finally, a system to assess the proposed strategy was set up (5). This plan led to the vaccination of a maximum of 450,917 dogs in 2005 (5). The apparition of various health crises in the livestock sector led to veterinary services control efforts to combat or prevent the diseases by intensifying surveillance and/or vaccination campaigns (sheep pox vaccination campaigns in 2002, 2004, and 2006, avian influenza surveillance in 2005 and 2006, bluetongue vaccination campaign in 2007, and PPR vaccination campaigns in 2008, 2009, and 2010) (34). This prevented the plan from reaching its objectives.

Despite the limited effect of these different plans on the status of rabies in general, they nonetheless laid the foundation for future actions: –

Creation of an interministerial rabies control committee.

Since 2014, WHO, OIE, and FAO—supported by the Institut Pasteur network—have launched an initiative to eradicate rabies in North Africa in general, and Morocco in particular, by around 2020. This initiative is supposed to materialize the implementation of the concept (71). Since the initial kickoff workshop in 2014, the actions in the framework of this initiative have not yet been communicated.

The parenteral vaccination of owned dogs in rural settings has been the key measure in rabies control programs in Morocco since 1911 (1). However, this measure was rapidly revealed to be insufficient in the light of the tiny proportion of dogs vaccinated compared to the size of the total dog population. The culling of dogs as a means of controlling the dog population was suggested in 1935 (2). This twofold mechanism, involving the vaccination of dogs and culling of stray dogs, is still carried out today in Morocco.

Several reasons for the failure of this strategy have been identified from 1938 on and are still relevant today: –

Vaccinating dogs against rabies has a moral and sentimental rather than economic aspect to it compared to other livestock vaccinations. Vaccinating dogs is considered a luxury (29).

Several judicious proposals have been put forward by various authors from 1935 on to improve the situation and are still relevant: –

Vaccinate community dogs that roam free (2).

Several authors (5, 13, 72–74) have underlined the importance of a good estimation of the dog population in the success of rabies control programs. According to WHO, the size of the dog population may be estimated through the human:dog ratio (59). Studies of the dog population carried out in Morocco in 1993 assessed the human:dog ratio at 5.93 in rural settings and 25.36 in urban settings. In 1999, the ratio was found to be 7.93 in rural settings and 80.94 in urban settings (5). More recently in 2013, estimations of this ratio for North Africa gave 3.84 in rural settings and 9.83 in urban settings (73) and for Africa in general, 7.40 in rural settings and 21.20 in urban settings (13).

To estimate the current dog population, we chose the mean of national dog population estimates obtained in 1990s and international estimates obtained in 2005 and 2013, giving a human:dog ratio of 6.14 in rural settings and 34.33 in urban settings. This value is no doubt biased but the bias is acceptable. By applying the calculated human:dog ratio and taking into account Moroccan demographic data (the Moroccan population being estimated in 2015 at 34,271,622 in all, including approximately 13,458,258 in rural settings and 20,813,364 in urban settings) (data from target populations of health programs. Health Ministry website http://www.sante.gov.ma), we may conclude that the dog population is estimate to stand at 2,798,126 (of which 2,191,930 in rural settings and 606,195 in urban settings). This number could be overestimated but we consider that it is better to overestimate the target population rather to underestimate it.

It should be noted that generally speaking, there are few data about Moroccan dog population features (sex ratio, mean age, and life expectancy of an owned or stray dog). Although Moroccan legislation requires dog owners to vaccinate their pets, it remains silent on the management of this population, as mentioned earlier. Neither does it inspire responsible ownership in order to prevent dogs creating a nuisance within the community.

Managing the dog population is a complementary measure in rabies control and reducing the dog population does not directly affect the transmissibility rate (R0, i.e., the reproduction number) of the rabies virus (75). This runs contrary to the idea that canine rabies can be eliminated by reducing the density of the dog population (59, 66). This reduction in density is frequently achieved through culling campaigns that often prove counterproductive and have a major impact on animal welfare (11). Indeed, dog owners frequently begin hiding their dogs, moving them to other areas, or indeed acquiring new dogs to replace those killed. This behavior is linked to the need for dogs, itself related to their function. In Morocco, dogs are mainly used as guard dogs, to watch over livestock (31%), a combination of both (87%) or to hunt (2%) (76). Dog movements help disseminate the rabies virus, as reported in Indonesia (75) and North Africa, including Morocco (62). Furthermore, dogs that are easy to vaccinate are those that are the easiest to cull, thus reducing the dog population’s immunity (66).

Dog sterilization campaigns are a key tool in the management of unwanted dogs. They reduce the trouble caused by dogs, along with their aggressive behavior and thus dog bites. They improve the human population’s acceptance of free-roaming dogs and improve the health and life expectancy of dogs in a roaming population (77). Sterilization would increase the effectiveness of vaccination campaigns by stabilizing the size of the dog population and reducing its renewal rate. It is an important complementary measure in a rabies control program whose key thrust is vaccination coverage (66).

Currently, Moroccan communes are responsible for taking measures to prevent animals from roaming free. They must collect, check, and impound stray dogs in compliance with article 50 of the Communal Charter (64).

However, these functions are not fulfilled in most towns and those communes where they have developed various systems: –

Some communes organize armed hunts with hunting associations following citizens’ complaints about the number of stray dogs. These hunting parties are held in daytime in urban settings. Communities and the press are increasingly hostile to this system (78, 79).

There are several possible ways of getting out of this situation, alone or in conjunction depending on local conditions: –

Stimulate the networking of animal protection associations through contract programs (82). Several animal welfare associations are active in different regions of Morocco, the oldest having been active since 1916 (83–90). One example is an association working in the town of Essaouira that captures, identifies, sterilizes, and vaccinates against rabies then frees the stray cats and dogs captured at the place they were found (91). This model could be followed and extended to other towns in order to manage the stray cat and dog population. The Department of Agriculture is very experienced in monitoring and implementing contract programs with professional associations (92), an experience that could be capitalized on to develop contract programs with animal protection associations in order to manage the stray cat and dog population while still complying with departmental prerogatives and respecting animal welfare criteria.

The most efficient means of preventing human rabies cases is to reach a 70% vaccination coverage of the dog population (12, 66). The vaccination coverage rate of the dog population in Morocco can be estimated by dividing the total number of vaccinated dogs by the total dog population, calculated by adding together the following two figures: –

The number of dogs vaccinated in rural settings, which corresponds to the number of dogs vaccinated during free mass vaccination campaigns organized by the government. The rural dog population represents 78% of the total dog population, as previously estimated in this study.

It should be noted that the vaccination coverage from 2009 to 2015 never exceeded 6% of the total dog population. Urban vaccination coverage fluctuates between 6.51 and 8.25%, while rural vaccination coverage fluctuates between 2.47 and 5.73% for the same period. The highest coverage rate in a rural setting was obtained during 2001–2010 NRCP, with 20.64% in 2005. The other national plans resulted in a maximum of 15.79% in 1994 and 11.41% in 1989. The data for urban vaccination coverage are not available before 2009. In any case, whether urban, rural, or total, the vaccination coverage rates are too low to break the transmission cycle of rabies virus. These data serve to confirm that since the first canine rabies vaccination in 1928, Morocco has only managed to vaccinate a tiny part of its dog population and is a very long way off the 70% vaccination coverage recommended by international organizations OIE and WHO (59, 70). Chevrier’s observation in 1965 that “this vaccination is of no prophylactic benefit compared to the total dog population, so the issue needs to be completely reviewed” is just as true today (30). This operation has always been carried out with the same strategy, using government officials for vaccinations in rural areas and private veterinarians in towns. In addition, all previous official rabies control plans have always targeted to vaccinate owned dogs population rather than targeting the whole sensitive population (i.e., total dog population) and those plans did not propose any strategy to vaccinate the stray dogs. This led to the described limited results of vaccination coverage and rabies control failure.

In our opinion, one of the ways of improving canine vaccination coverage would be to involve private veterinarians in the free government-run vaccination campaigns, whether in rural or urban settings, as part of a public–private partnership. The synergy between ONSSA and private veterinarians during an action program to vaccinate sheep and cattle was successful in tackling various livestock diseases (PPR vaccination campaigns in 2008, 2009, and 2010; bluetongue vaccination campaign in 2007; sheep pox vaccination campaigns in 2011 and 2013, and foot-and-mouth disease vaccination campaign in 2015) (34). This public–private partnership managed on more than one occasion to successfully vaccinate 19.5 million sheep and 3.2 million cattle (92) within 3–4 months, resulting in a vaccination coverage of about 97% (34). The pathway to participation of private veterinarians has already been cleared through a decree establishing government remuneration of veterinarians in the private sector for the vaccination of dogs and cats in January 2015 (99).

Oral vaccination is another promising possibility currently under investigation for dogs. WHO has proposed various application scenarios, such as door-to-door vaccination, distribution at a central point, or a wildlife model (100). The latter involves jettisoning baits from aircraft, which is not very practicable for the oral vaccination of dogs. Unlike wildlife, the dog’s habitat is closely linked to that of humans, making aerial distribution such as practiced in un- or little-populated areas where wildlife live unrealistic for dogs. Unlike injectable rabies vaccines, which are inactivated and often contain adjuvants, oral rabies vaccines are live attenuated vaccines or recombinant protein vaccines. Several oral rabies vaccines have market authorizations, yet only two are considered sufficiently safe by WHO (59, 100) to be used in proximity to people. One is Rabigen SAG2™, produced by Virbac SA, France (101), and the other is Raboral V-RG^®, produced by Merial Inc., USA (102). The other commercial vaccines have residual virulence that can induce rabies, in target and non-target species (103, 104).

Studies have been carried out on the use of V-RG on dogs in Morocco, investigating the appetence of the bait and its efficacy under controlled conditions, but the study results were limited (49, 105). This had already been observed by other authors (72). Further research would be beneficial to investigate the efficacy of this vaccine on dogs and cats.

The results of a pilot study carried out in Morocco on the use of SAG2 for oral vaccination of dogs in field conditions were promising. The dog population in the study zone was composed of 70% of owned dogs and 30% of stray dogs. Using the door-to-door model (59), 77% of owned dogs ate the bait. Using the wildlife immunization model (59) in stray dogs, up to 73% of baits disappeared and 68% of the capsules containing the SAG2 vaccine were found pierced (106). Further research is needed to fine-tune the distribution strategy before large application in the field.

In our opinion, the oral vaccination of dogs is a way forward in conjunction with parenteral vaccination as recommended by WHO (59). It would reach stray dogs or dogs that are inaccessible due to their aggressive behavior and could be organized during mass parenteral vaccination campaigns. It would also be possible to distribute baits to well-informed owners so that they themselves give their dog the bait (on the condition that is in individual wrapping and kept at 4°C for no more than a few days), with strict instructions on giving the bait as soon as it has been opened. If not consumed straight away, it must be destroyed.

The use of new technologies has given good results by allowing real-time monitoring of mass vaccination campaigns (107). Several parameters can be assessed in real time, such as the number of dogs vaccinated, the proportion of dogs vaccinated compared to the total population, the GPS position of vaccination locations, and a map of the vaccination coverage per region for the whole country (107, 108). This should be able to be used in Morocco, one of the main advantages being that it would enable resources and vaccination teams to be redeployed in real time without having to wait for the end of a campaign before drawing conclusions.

All these difficulties underline the peculiarities of rabies compared to other livestock diseases, where often just one vaccination campaign is enough to improve the situation. For rabies, substantial efforts have to be made over several consecutive years on a sufficient large range of dog population, each interruption losing the benefits accrued up to then. This shows the importance of political determination and coordinated efforts. Rabies should never be accepted as banal. Even though it is not a disease with a direct economic impact (dogs generally not having an “economic” value), political efforts must be kept up over a long period so that the enthusiasm of vaccination teams does not wane year after year. Vaccination initiatives must be maintained in the light of an ever-increasing dog population and efforts should not be allowed to be diverted to other health priorities.

The “One World, One Health” concept was initiated in 2008 by FAO, OIE, and WHO with the support of the United Nations Children’s Fund, the United Nations System Influenza Coordination, and the World Bank (109). It aims to develop a joint strategic network for coordinating medical, veterinarian, and environmental health policies to face up to the risks associated with the emergence or reemergence of zoonoses (109, 110). The major advantage of this concept lies in the economies of scale afforded through the efficiency of control and elimination measures, which is why it is so advantageous for low-income nations (66).

Latin America is a successful example of the “One World, One Health” concept as regards rabies. The strong political will of all the countries in that region was channeled into national public health and animal health action plans. Mass dog vaccination campaigns were held (59). The cooperation with NGOs, animal welfare organizations, and a close public–private partnership supported by efficient communication with local communities which were also heavily involved were the keys to the success of this rabies elimination program (66). Results were visible after a few years, by which time animal and human rabies cases had dropped by 90% (59).

The bases for this “One World, One Health” approach already exist in Morocco. The interministerial committee on rabies control is just one proof. The action of this committee should be supported by new legislation that gives it broader powers. Kenya, for example, created a “One Health Office” in 2011 in order to develop control strategies for the country’s priority zoonoses, including rabies (111).

Since 2009, Morocco has celebrated World Rabies Day (112), an initiative launched in 2007 by the Global Alliance for Rabies Control. Held on September 28 each year, World Rabies Day seeks to focus the attention of the international community on rabies prevention and control measures (113). The World Rabies Day events from 2009 to 2013 were organized jointly by the National Food Safety Office, ONSSA, and the Hassan II Agronomics and Veterinary Institute, with the participation of other ministerial departments such as the Moroccan Ministry of Health, the Ministry of the Interior, the Ministry of National Education, and the Ministry of Islamic Affairs, in addition to local authorities, the Moroccan Association of Veterinary Professors–Researchers, the Society for the Protection of Animals and Nature along with the media. Various rabies-related actions were held on these occasions, including a rabies science day, the vaccination of dogs, information on rabies targeting elected officials in the communes, Friday sermon on rabies throughout all the mosques in Morocco, educating and informing primary school children about rabies, awarding of a prize to the journalist having done the best report on rabies, a radio broadcast, and inclusion on the news of the main TV channel (112). All these local and national events have raised awareness among the general public, especially young people, and will bear fruit in the long term.