The first case of AIDS was diagnosed in 1981 in the United States. Since then, AIDS patients have been reported all over the world, in particular, from Asia, South America and sub-Saharan Africa. It is estimated that there are 33.3 million (31.4–35.3 million) adults and children living with HIV, and it has been shown that there are about 2.6 million (2.3–2.8 million) people and about 370 000 (230 000–510 000) children who are newly infected with HIV. It is surmised that there are 1.8 million (1.6–2.1 million) AIDS-related deaths worldwide annually .
Parasites are one of the main causative agents that can worsen the situation of HIV-infected patients and are one of the significant causes of morbidity and mortality in HIV/AIDS patients.
Recent estimates showed that at least one- quarter of the world's population is infected with enteric parasites, and most of these people live in the developing countries. Currently, intensive expansion of the HIV/AIDS pandemic has changed the fauna of the intestinal parasites in the world, especially in developing countries, and has caused an expansion and renovation of newly emerging intestinal parasites [2–5].
In HIV patients, intracellular protozoa causing diarrhoea (including Isospora belli, Cryptosporidium parvum and Cyclospora spp.) are the main causative agents , and among extracellular parasites, Entamoeba histolytica, Giardia intestinalis and Strongyloides stercoralis are the most prominent . Among intracellular parasites, there is a higher prevalence of Cryptosporidium spp. and S. stercoralis in HIV-positive individuals, rather than among extracellular parasites . Leishmaniasis and toxoplasmosis are recognized as the main opportunistic infections in HIV-infected patients .
It has been shown that parasitic infections could potentiate HIV replication and accelerate disease progression [9,10]. Immunological studies have shown that T-helper 1 (Th1)-type immune responses are related to viral diseases and Th2-type immune responses are associated with helminth infections, whereas in parasitic infections there is a shift from Th1-type to Th2-type response; this latter change may promote HIV infection and progression [9,11].
Enteric parasites in HIV/AIDS patients
Cryptosporidiosis and isosporiasis are identified as the two most common causes of diarrhoea and contribute to a public health problem among AIDS patients . In immunocompetent patients, cryptosporidiasis is a self-limiting diarrhoea, whereas in immunodeficient patients, it can cause a severe, prolonged gastroenteritis. The lack of effective therapy for cryptosporidial-cause diarrhoea can lead to dehydration and death [12,13]. Reports from 1997 showed that diarrhoea is seen in 30–60% of AIDS patients in developed countries, and from 2002 about 90% of AIDS patients in developing countries . The prevalence of cryptosporidiosis among HIV-positive patients ranges from 0 to 100% . Cryptosporidiosis is found in AIDS patients when the CD4+ cell count is below 200 cells/μl.
Babatunde and Salami  showed that the prevalence of cryptosporidiosis and isosporiasis amongst HIV patients was about five times higher than amongst HIV-negative patients, whereas this ratio for cyclospora was 1.7. A cross-sectional study from January 2007 to December 2008 in Ilorin, Nigeria, found that both opportunistic and non-opportunistic intestinal parasitic prevalence were two and a half times higher among the HIV-seropositive patients than amongst the seronegative ones . Alemu et al., in a cross-sectional 2-month study conducted in Bahir Dar City, northwest Ethiopia in 2009, considered that C. parvum was the most prominent opportunistic parasite in HIV-seropositive patients (62.6%, 82/131), followed by I. belli (22.1%) and Blastocystis hominis (15.3%).
Pavie et al. reported a 17% prevalence of intestinal parasitic infection in a population of advanced HIV-infected patients with combination antiretroviral therapy (ART) in France between May 2003 and June 2006. Various types of intestinal parasites were reported, but the majority were Microsporidia, Cryptosporidia, Giardia, S. stercolaris and I. belli (84%, 21/25). Despite the availability of combination ART, parasitic pathogens remained high in patients. Indeed, 10% of the patients without diarrhoea had intestinal parasites detected .
Missaye et al. reported that in northeast Ethiopia, the total prevalence of intestinal protozoa in HIV-positive patients before ART (pre-ART) was 39% and among these, the prevalence of protozoa was 31%, helminthic infection 7.4%, and both protozoal and helminthic infections 0.7%; the prevalence of opportunistic intestinal parasites was 2.2%, and among these, 1.5% belonged to Cryptosporidium spp. and 0.7% to I. belli. The prevalence of intestinal protozoa among non-antiretroviral-treated patients was 17.6%, out of which 12.5% were protozoal and 5.1% were helminthic infections. No opportunistic parasites and mixed infections were seen in this group. E. histolytica/dispar and Ascaris lumbricoides, with respective prevalence of 5.1 and 2.2%, respectively, were the most prevalent protozoal and helminthic parasites among patients receiving ART. The overall prevalence of intestinal protozoa in the pre-ART (39%) and antiretroviral treatment groups (17.5%) indicates a statistically significant difference between the groups (P < 0.001).
A report from 2012, which was based on a study conducted for a 2-month period in 2010 in Equatorial Guinea, showed an infection rate of 81.5% by one or more intestinal parasites among HIV-positive participants . Among the participants, 62.3% had pathogenic helminthes such as Trichiuristrichiura, A. lumbricoides, Schistosoma intercalatum/guineensis, S. stercoralis and hookworms. Pathogenic protozoa such as E. histolytica/dispar and Giardia caused 47.7% (124/260) of the infections. Opportunistic protozoa (Escherichia coli, B. hominis, Cryptosporidium spp., Endolimax nana, Pentatrichomonas hominis, Chilomastix mesnili, Iodamoeba bütschlii and Entamoeba hartmanni) were found in 35.0% of the patients .
Lehman et al., in a prospective study conducted from January to December 2011 in the Cameroon, reported that the prevalence of Cryptosporidium spp. and E. histolytica/dispar among HIV patients was 7.4 and 3%, respectively. The highest parasite counts (P = 0.035) and diarrhoea (P < 0.0001) were found in patients with CD4+ below 200 cells/μl. S. stercoralis, T. trichuira and I. belli were only seen in diarrhoeal samples.
Microsporidia were detected in 21/247 (8.5%) of stool samples from HIV-infected individuals; these patients were three times more likely to acquire Microsporidia than the non-infected individuals .
Another study reported prevalences of 13.9% (78/561) and 8.5% (25/295) for Microsporidia in HIV-positive and HIV-negative patients, respectively. The results clearly showed the significant association between the presence of microsporidial infection and HIV infection. The prevalence of Enterocytozoon bieneusi was 7.0% and Vittaforma-like was 8.2% in faecal specimens from HIV-positive patients .
Malaria in HIV/AIDS patients
It is considered that almost 2.5 million deaths were attributable to malaria and/or HIV-1 infection in 2009 . Recent studies have demonstrated that these two pathogens can negatively affect each other in several respects [26,27]. Malaria and HIV overlap geographically in sub-Saharan Africa, south-east Asia and South America .
During severe bouts of Plasmodium falciparum infection, the level of HIV RNA increases . Repeated malarial infections are related to a rapid reduction in CD4+ T-lymphocyte counts during an HIV-1 infection. All these findings show that symptomatic P. falciparum infections may stimulate progression of HIV . The risk of malarial infection is increased in HIV-1 patients [31,32]. Moreover, individuals with HIV/malaria are more likely to suffer from higher morbidity, higher mortality and higher relapse rates . Additionally, acute malaria/HIV co-infection can lead to an increase in viral load and a reduction in CD4+ cell count, and these viral load and CD4+ cell count changes can result in the treatment failure for malaria [34,35].
Blood smear-positivity for P. falciparum was significantly higher in HIV-infected individuals compared to HIV-negative patients (9.9 vs. 5.1%) .
A study in Malawi in 2013 showed a viral load of HIV-1 in infected adults with acute uncomplicated malaria to be seven-fold higher than in the HIV-1-infected individuals without malaria . Earlier in-vitro studies had showed that peripheral blood mononuclear cells infected by HIV-1 exposed to malaria antigens or malaria pigment had 10–100-fold higher viral burden .
The immune response of children with HIV infection to multiple malaria antigens is reduced, and HIV can modify the age-related acquisition of antibodies to P. falciparum. Thus, both the magnitude and breadth of antibody response can be impaired by HIV . It seems that the association between HIV and malaria depends on both age and transmission intensity. Therefore, apparently, the interaction between malaria and HIV can be both bidirectional and synergistic.
An Indian study showed that 13 (7.6%) out of the 171 malaria patients and 521 (1.81%) out of the 28 749 blood bank donors were HIV-1 and HIV-2-seroreactive, and in some co-infection with malaria and HIV-1 occurred .
A case–control study in Uganda reported that HIV-1 infection was seen among 9% of children with cerebral malaria compared to 2.3% in uncomplicated malaria and 2.5% in children with no malaria . In South Africa, 17% of the children with severe malaria had HIV, whereas only 7.5% of the children with uncomplicated malaria were infected by HIV. Another study in Kenya showed a 12% prevalence among children with severe malaria .
Infected pregnant women with HIV and/or malaria give birth to babies with higher risk of foetal anaemia and cord blood malarial parasitaemia. It was shown that HIV/malaria co-infection can predict adverse perinatal outcomes .
Toxoplasma in HIV/AIDS patients
Since the mid-1980s, this disease has attracted increased attention. Cerebral toxoplasmosis is considered to be the most common neurological opportunistic infection in HIV-infected individuals. Toxoplasmosis can be presented as central nervous system (CNS) involvements, chorioretinitis, pneumonitis and haemodynamic abnormalities in immunocompromised patients .
The prevalence rates of latent toxoplasmosis in HIV patients varies widely (3–97%) [42–45].
Ibebuike et al., in 2012, reported a rare case of toxoplasmosis in an 11-month-old HIV/AIDS female infant.
A retrospective study in the south of Iran between 2003 and 2005  revealed that the seroprevalence of toxoplasmosis among HIV/AIDS patients was 18.2% (38/208). Moreover, 89.6% of the patients presented with toxoplasmosis without encephalitis and four (10.4%) patients showed toxoplasmosis with encephalitis.
Csep and Dra[Combining Breve]ghici , in 2013, showed that the seroprevalence of Toxoplasma gondii antibody among HIV patients in Bihor County, Romania, during the year 2012, was 33.3%.
A Moroccan study reported that 62.1% of HIV-infected patients had anti-T. gondii IgG .
The prevalence of toxoplasmosis among the HIV patients in Algeria was 51.56% . The seroprevalence of toxoplasmosis in the HIV-infected patients is reported as 5.4% in Japan  and 77.4% in northern Iran .
In Prague (Czech Republic), it was found that 396 (41.4%) men and 78 (44.8%) women out of the 1130 HIV-infected patients were infected with T. gondii before HIV diagnosis . Pregnant women in Mozambique showed an overall occurrence of anti-Toxoplasma IgG antibodies among HIV-positive patients (31.3%, 18/58) and (10.9%, 10/92) in HIV-negative patients . It was reported that of the 130 HIV-positive patients in Uganda, 54% were antibody-positive, whereas 23% were detected with active infection and parasites in their peripheral blood .
Visceral leishmaniasis in HIV/AIDS patients
Visceral leishmaniasis is a worldwide disseminated infection. The first case of leishmaniasis associated with HIV infection was reported in 1985, and since then, 35 countries have reported cases of co-infection . The geographical overlap of the two diseases can affect the incidence of Leishmania/HIV co-infection . In visceral leishmaniasis-endemic areas, L. infantum co-infection has become the third most frequent infection in HIV-infected individuals . Since 1994, the incidence of Leishmania/HIV co-infection has been monitored by a surveillance network consisting of 16 institutions  in four countries: France, Italy, Portugal and Spain . Spain recorded the highest number of cases .
HIV infection increases the probability of relapse and decreases the likelihood of therapeutic response; on the contrary, visceral leishmaniasis promotes clinical progression of HIV disease and the development of AIDS-defining conditions. Both diseases influence the cellular immune response synergistically. Atypical presentations of leishmaniasis are shown in HIV patients, including visceralization of cutaneous leishmaniasis (CL) and cutaneous involvement in visceral leishmaniasis . Leishmania/HIV co-infection has been reported in 35 countries; it is currently reported in 2–12% of all visceral leishmaniasis cases. The global incidence is underestimated, because visceral leishmaniasis is not on the Centers for Disease Control and Prevention list of opportunistic infections . Most co-infections are reported from Brazil. In Brazil, 620 000 people are living with HIV. The cases of visceral leishmaniasis from 700 cases in 1980 increased to 3500 in 2005, and for tegumentary leishmaniasis, from 4000 cases in 1980 to 32 000 in 2005 .
The number of co-infection cases has increased in Africa due to social problems. In some parts of Ethiopia, 30% of all visceral leishmaniasis patients are also infected with HIV. In Asia, co-infections are increasingly being reported in Bangladesh, India and Nepal as 7000, 32 800 and 3000, respectively [62,63]. In southern Europe, to the end of 2001, a total of 1911 co-infection cases had been reported to the WHO database from France, Italy, Portugal and Spain. Two hundred and forty-one new cases were reported to WHO during the period 2001–2006. Germany, Greece, Switzerland and the United Kingdom reported sporadic imported cases .
From 2000 to 2006, in the Kala-Azar Medical Research Centre in Muzaffarpur (Bihar), the number of HIV-positive patients increased by 50% as the visceral leishmaniasis/HIV co-infection rate increased from 0.88% in 2000 to 2.18% in 2006. In 2006, the visceral leishmaniasis/HIV co-infection rate was reported to be almost 2.48% in India. In a study conducted in 39 hospitals in Nepal, 5.7% of the patients had visceral leishmaniasis/HIV co-infection . No data on Leishmania/HIV co-infection are available from Bangladesh, but it is likely to be high as it shares borders with India and Nepal .
In the Humera region of northwest Ethiopia, 40% of the visceral leishmaniasis patients were also co-infected with HIV in 2006, representing an increase of 21.5% from 1999 . The fatality rate of visceral leishmaniasis/HIV-infected patients was reported to be four times higher than those with visceral leishmaniasis, but not HIV infection. In Kenya, in 2006, only 15 cases of visceral leishmaniasis/HIV co-infection were reported, but there is likely to be considerable under-reporting of the real prevalence rate . A study from Cameroon, in 2012, showed a 4.8% rate of CL/HIV co-infection . According to the Brazilian Ministry of Health (2011), the rate of 6.5% is currently estimated for HIV/visceral leishmaniasis co-infection . However, there was a reduction in the number of visceral leishmaniasis and HIV/visceral leishmaniasis cases in 2009 and 2010; the HIV/visceral leishmaniasis proportion still remained high in 2010 (17.4%). In Brazil, 57% of the HIV patients were diagnosed after visceral leishmaniasis became apparent. The Ministry of Health has recommended that all patients with visceral leishmaniasis be tested for HIV .
In northeast Iran, in March to December of 2012, nine (18.4%) out of the 49 cases of HIV/AIDS had anti-L. infantum antibodies with a titre of 1 : 100 . In a study conducted in Brazil, in 2012, the prevalence of asymptomatic Leishmania spp. was estimated to be 20.2% .
The numbers of CD4+ T lymphocytes in HIV/Leishmania patients were significantly (P < 0.001) lower than in the HIV-1-infected patients without leishmaniasis, although CD4+ T-cell counts in tegumentary leishmaniasis/HIV patients were similar to the HIV-1-infected patients without leishmaniasis .
A survey in 2012, of 146 CL patients conducted in the Mokolo region, showed that seven patients had antibodies to HIV (two HIV-1 and five HIV-1/HIV-2), representing 4.8% of the patients with active CL infection .
Parasite/HIV co-infection must be considered as a dilemma because co-infection occurs in highly endemic disease areas. On the contrary, parasitic diseases are increasingly neglected.
There are very few published studies that have evaluated the prevalence rate of parasite/HIV co-infection. With the emergence of AIDS, parasitic diseases have gained significance, as they can be one of the important causes of morbidity and mortality among HIV patients.
It is worth mentioning that the prevalence of parasite/HIV co-infection tends to be far higher than those reported. HIV-infected populations are more susceptible to co-infection than HIV-negative individuals, particularly those with poor personal hygiene habits. Despite the potential risks related to parasite/HIV co-infection, little is known of the interaction between different types of parasites and HIV, especially in high-risk communities.
We propose that various types of parasitic infection should be considered in terms of their differential diagnosis, clinico-epidemiology, prevention and treatment in HIV-infected patients.
Conflicts of interest
There are no conflicts of interest.
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