Abstract

Cryptosporidium is an intracellular protozoan parasite, globally distributed and capable of infecting various vertebrate species, including humans as well as domestic and wild animals. Cryptosporidium is increasingly gaining attention as a human and an animal pathogen mainly due to its dominant involvement in worldwide waterborne outbreaks. The present paper reviews the current knowledge and understanding of Cryptosporidium spp. in terrestrial and water animals in Azerbaijan.

Highlights

  • First review on knowledge and understanding of Cryptosporidium spp. in terrestrial and water animals in Azerbaijan.

  • First review zoonotic Cryptosporidium species in Azerbaijan.

  • Crypto livestock, wildlife, amphibians, birds, and mammals.

  • An extensive report based on a comparative analysis of morphometric parameters of Crypto oocysts.

  • High prevalence rates in domestic and wild animals.

Graphical Abstract

Graphical Abstract
Graphical Abstract

INTRODUCTION

Cryptosporidium is an intracellular protozoan parasite and is a major cause of gastroenteritis (cryptosporidiosis) worldwide. Cryptosporidium is a globally distributed genus of diarrheal pathogens capable of infecting various vertebrate species, including humans as well as domestic and wild animals (Xiao et al. 2004; Plutzer & Karanis 2009). To date, a total of 44 Cryptosporidium and Cryptosporidium-like species have been described from animals and humans (Table 1).

Table 1

Cryptosporidium and Cryptosporidium-like species with information on organ location and morphometric characters of oocysts reported from animals

NSpecies nameAuthors reported for first timeType hostMajor hostSite of infectionDimension (μm) L (average) × W (average)L/W (Length/width)References
123456789
Cryptosporidium and Cryptosporidium-like parasites reported from fish 
C. nasorum Hoover et al. (1981)  Lipstick tang (Naso liburatusFish Intestine NR NR Levine (1980), Ryan (2010), Šlapeta (2013)  
C. cichlidis=Piscicryptosporidium cichlidis Paperna & Vilenkin (1996)  Hybrid fry and fingerling tilapia (Oreochromis aureus × Oreochromis nicloticusFish Stomach 4.0–4.7, 2.5–3.5 NR Ryan (2010), Šlapeta (2013)  
C. reichenbachklinkei=Piscicryptosporidium reichenbachklinkei Paperna & Vilenkin (1996)  Reared gouramis (Trichogaster leeriFish Stomach 2.4–3.18, 2.4–3.0 NR Šlapeta (2013)  
C. molnari Alvarez-Pellitero & Sitjà-Bobadilla (2002)  Gilthead sea bream (Sparus aurata) and the European sea bass (Dicentrarchus labraxFish Stomach and small intestine 3.23–5.45 (4.72) × 3.02–5.04 (4.47) 1–1.17 (1.05) Alvarez-Pellitero & Sitjà-Bobadilla (2002)  
C. scophthalmi Alvarez-Pellitero et al. (2004)  Turbot (Scophthalmus maximusFish Intestine and stomach 3.7–5.03 (4.44) × 3.03–4.69 (3.91) 1.05–1.34 (1.14) Alvarez-Pellitero et al. (2004)  
C. huwi Ryan et al. (2015)  Guppy (Poecilia reticulataFish Stomach 4.4–4.9 (4.6) × 4.0–4.8 (4.4) 0.92–1.35 (1.04) Ryan et al. (2015)  
Cryptosporidium species reported from amphibians 
C. fragile Jirku et al. (2008)  Black-spined toads, (Duttaphrynus melanostictusNR Stomach 5.5–7.0 (6.2) × 5.0–6.5 (5.5) NR Jirku et al. (2008)  
Cryptosporidium species reported from reptiles 
C. serpentis Levine (1980)  Elaphe gualta, E. suboclaris, Sanzinia madagascarensis (Snakes) Snakes and lizards Stomach 5.6–6.6 (6.2) × 4.8–5.6 (4.2) 1.04–1.33 (1.16) Plutzer & Karanis (2009), Ryan et al. (2014)  
C. varanii=C. saurophilum Pavlásek et al. (1995), Koudela & Modry (1998)  Varanus prasinus (Emeriald monitor), Shneider's skinks (Eumeces schneideriLizards Stomach and small intestine 4.4–5.6 (5.0) × 4.2–5.2 (4.7), 4.4–5.6 (5.0) × 4.2–5.2 (5.3) 1.05–1.12 (1.09) Koudela & Modry (1998), Ryan et al. (2014)  
10 C. ducismarci Traversa (2010)  Tortoises Tortoises, turtles, other reptiles NR 4.4–5.4 (5.0) × 4.3–5.3 (4.8) 1.1 ± 0.03 Ježková et al. (2016)  
11 C. testudines Ježková et al. (2016)  Russian tortoises (Testudo horsfieldii, Gray) Tortoises NR 5.8–6.9 (6.4) × 5.3–6.3 (5.9) 1.1 ± 0.05 Ježková et al. (2016)  
Cryptosporidium species reported from birds 
12 C. meleagridis Slavin (1955)  Melleagris gallopova (Turkey) Birds and humans Small intestine 4.5–6.0 (5.0) × 4.2–5.3 (4.4) 1.0–1.3 (1.3) Plutzer & Karanis (2009), Ryan et al. (2014)  
13 C. baileyi Current et al. (1986)  Gallus gallus (Chicken) Birds Bursa, cloacae, trachea 5.6–7.5 (6.4) × 4.8–5.75 (4.8) 1.1–1.4 (1.3) Current et al. (1986), Plutzer & Karanis (2009)  
14 C. galli Pavlásek (1999), Ryan et al. (2003)  Chickens Passeriformes, Phasianidae, Fringillidae, and Icteridae Proventriculus 8.0–8.5 (8.25) × 6.2–6.4 (6.3) 1.30 Ryan et al. (2003)  
15 C. avium Holubová et al. (2016)  Red-crowned parakeets (Cyanoramphus novaezealandiaeBudgerigar, hens Ileum and cecum 5.30–6.90 (6.26) × 4.30–5.5 (4.86) 1.14–1.47 (1.29) Holubová et al. (2016)  
16 C. proventriculi Holubová et al. (2019)  Psittaciformes (Birds) Birds Proventriculus and ventriculus 7.4 × 5.8 NR Holubová et al. (2019)  
Cryptosporidium species reported from mammals 
17 C. muris Tyzzer (1907)  Hause mause (Mus musculusRodents Stomach 8.0–9.0 (8.4) × 5.6–6.4 (6.1), 7.0–9.0 (8.1) × 5.0–6.5 (5.9) 1.25–1.61 (1.38) 1.17–1.7 (1.36) Plutzer & Karanis (2009), Ryan et al. (2014)  
18 C. tyzzery Tyzzer (1912), Ren et al. (2012)  Domestic mice (Mus musculusRodents Jejunum and ileum 4.64 ± 0.05 × 4.19 ± 0.06 1.11 ± 0.02 Ren et al. (2012)  
19 C. proliferans Kváč et al. (2016)  Northeast African mole-rat (Tachyoryctes splendensDonkey, Sciurus eastern grey squirrel, African buffalo, horse Stomach, specifically the glandular part 6.8–8.8 (7.7) × 4.8–6.2 (5.3) 1.48 Kváč et al. (2016)  
20 C. apodemi Čondlová et al. (2018)  Striped field mouse (Apodemus agrariusYellow-necked mice (Apodemus flavicollisIntestine 3.9–4.7 (4.2) × 3.8–4.4 (4.0) 1.0–1.06 (1.03) Čondlová et al. (2018)  
21 C. ditrichi Čondlová et al. (2018)  Yellow-necked mice (Apodemus flavicollisMouse (Mus musculus), human (Homo sapiensSmall intestine – jejunum and ileum 4.5–5.2 (4.7) × 4.0–4.6 (4.2) 1.0–1.2 (1.12) Čondlová et al. (2018)  
22 C. occultus Kváč et al. (2018)  Wild brown rats, mice (Rattus norvegicus), Mongolian gerbils (Meriones unguiculatusRodents Colon 5.20 × 4.94 NR Kváč et al. (2018)  
23 C. alticolis Horčičková et al. (2019)  Common voles (Microtus arvalisVoles Small intestine 5.4 × 4.9 NR Horčičková et al. (2019)  
24 C. macroti Horčičková et al. (2019)  Common voles (Microtus arvalisVoles Large intestine 4.3 × 4.1 NR Horčičková et al. (2019)  
25 C. cuniculus Inman & Takeuchi (1979), Robinson et al. (2010)  European rabbits (Oryctolagus cuniculus) and humans (Homo sapiensRabbits Small intestinal 5.55–6.40 (5.98) × 5.02–5.92 (5.38) 1.1 Robinson et al. (2010)  
26 C. rubeyi Li et al. (2015)  Squirrel (Spermophilus beecheyi, Spermophilus beldingi, Spermophilus lateralisSquirrels NR  4.4–5.0 (4.67) × 4.0–5.0 (4.34) 1.08 Li et al. (2015)  
27 C. felis Iseki (1979)  Felis catis (Cat) Cat Small intestine 6.0–5.0 (5.0) × 5.0–4.5 (4.5) NR Iseki (1979), Plutzer & Karanis (2009), Ryan et al. (2014)  
28 C. canis Fayer et al. (2001)  Canis familiaris (Dog) Dogs Small intestine 4.95 × 4.75 1.05 Fayer et al. (2001), Plutzer & Karanis (2009)  
29 C. wrairi Vetterling et al. (1971)  Cavia porcellus (Guinea pigs) Guinea pigs Small intestine 4.8–5.6 (5.4) × 4.0–5.0 (4.6) 1.17 Plutzer & Karanis (2009), Ryan et al. (2014)  
30 C. homai Zahedi et al. (2017)  Cavia porcellus (Guinea pigs) NR NR NR NR Zahedi et al. (2017)  
31 C. suis Ryan et al. (2004)  Sus scrofa (Pig) Pigs The small and large intestine 4.9–4.4 (4.6) × 4.0–4.3 (4.2) 1.1 Ryan et al. (2004)  
32 C. scrofarum Kváč et al. (2013)  Sus scrofa (Pig) Human, calf, wild boar Duodenum, jejunum, ileum, cecum, colon 4.81–5.96 (5.16) × 4.23–5.29 (4.83) 1.07 ± 0.06 Kváč et al. (2013)  
33 C. parvum Tyzzer (1912)  Bos taurus (Cattle) Ruminants, cattle other livestock, humans Small intestine 4.5–5.4 (4.9) × 4.2–5.2 (4.4) 1.0–1.13 (1.1) Plutzer & Karanis (2009), Ryan et al. (2014)  
34 C. andersoni Lindsay et al. (2000)  Bos taurus (Cattle) Cattle, camel Abomasum 6.0–8.1 (7.4) × 5.0–6.5 (5.5) 1.07–1.50 (1.35) Lindsay et al. (2000)  
35 C. bovis Fayer et al. (2005)  Bos taurus (Cattle) Cattle Small intestine 4.76–5.35 (4.89) × 4.17–4.76 (4.63) 1.06 Fayer et al. (2005)  
36 C. ryanae Fayer et al. (2008)  Bos taurus (Cattle) Cattle NR 2.94–3.68 (3.73) × 2.94–4.41 (3.16) 1.18 Fayer et al. (2008)  
37 C. ubiguitum Fayer et al. (2010)  Bos taurus (Cattle) Ruminants, rodents, carnivores, primates, humans NR 4.71–5.32 (5.04) × 4.33–4.98 (4.66) 1.08 Fayer et al. (2010)  
38 C. pestis Slapeta (2006)  Bos taurus (Cattle) NR NR NR NR Šlapeta (2013)  
39 C. xiaoi Fayer & Santín (2009)  Ovis aries (Sheep) Sheep and goats NR 2.94–4.41 (3.94) × 2.94–4.41 (3.44) 1.15 Fayer & Santín (2009)  
40 C. erinacei Kváč et al. (2014)  European hedgehog (Erinaceus europaeusHedgehogs NR 4.5–5.8 (4.9) × 4.0–4.8 (4.4) 1.02–1.35 (1.13) Kváč et al. (2014)  
41 C. fayeri Ryan et al. (2008)  Red kangaroo (Macropus rufusMarsupials Small intestine 4.5–5.1 (4.9) × 3.8–5.0 (4.3) 1.02–1.18 (1.14) Ryan et al. (2008)  
42 C. macropodum Power & Ryan (2008)  Eastern grey kangaroos (Macropus giganteus). Marsupials Small intestine 5.0–6.0 (5.4) × 4.5–6.0 (4.9) 1.1 Power & Ryan (2008)  
43 C. hominis Morgan-Ryan et al. (2002)  Homo sapiens (Humans) Humans Small intestine 4.4–5.9 (5.2) × 4.4–5.4 (4.86) 1.0–1.09 (1.07) Ryan et al. (2002)  
44 C. viatorum Elwin et al. (2012)  Homo sapiens (Humans) Humans NR NR NR Elwin et al. (2012)  
NSpecies nameAuthors reported for first timeType hostMajor hostSite of infectionDimension (μm) L (average) × W (average)L/W (Length/width)References
123456789
Cryptosporidium and Cryptosporidium-like parasites reported from fish 
C. nasorum Hoover et al. (1981)  Lipstick tang (Naso liburatusFish Intestine NR NR Levine (1980), Ryan (2010), Šlapeta (2013)  
C. cichlidis=Piscicryptosporidium cichlidis Paperna & Vilenkin (1996)  Hybrid fry and fingerling tilapia (Oreochromis aureus × Oreochromis nicloticusFish Stomach 4.0–4.7, 2.5–3.5 NR Ryan (2010), Šlapeta (2013)  
C. reichenbachklinkei=Piscicryptosporidium reichenbachklinkei Paperna & Vilenkin (1996)  Reared gouramis (Trichogaster leeriFish Stomach 2.4–3.18, 2.4–3.0 NR Šlapeta (2013)  
C. molnari Alvarez-Pellitero & Sitjà-Bobadilla (2002)  Gilthead sea bream (Sparus aurata) and the European sea bass (Dicentrarchus labraxFish Stomach and small intestine 3.23–5.45 (4.72) × 3.02–5.04 (4.47) 1–1.17 (1.05) Alvarez-Pellitero & Sitjà-Bobadilla (2002)  
C. scophthalmi Alvarez-Pellitero et al. (2004)  Turbot (Scophthalmus maximusFish Intestine and stomach 3.7–5.03 (4.44) × 3.03–4.69 (3.91) 1.05–1.34 (1.14) Alvarez-Pellitero et al. (2004)  
C. huwi Ryan et al. (2015)  Guppy (Poecilia reticulataFish Stomach 4.4–4.9 (4.6) × 4.0–4.8 (4.4) 0.92–1.35 (1.04) Ryan et al. (2015)  
Cryptosporidium species reported from amphibians 
C. fragile Jirku et al. (2008)  Black-spined toads, (Duttaphrynus melanostictusNR Stomach 5.5–7.0 (6.2) × 5.0–6.5 (5.5) NR Jirku et al. (2008)  
Cryptosporidium species reported from reptiles 
C. serpentis Levine (1980)  Elaphe gualta, E. suboclaris, Sanzinia madagascarensis (Snakes) Snakes and lizards Stomach 5.6–6.6 (6.2) × 4.8–5.6 (4.2) 1.04–1.33 (1.16) Plutzer & Karanis (2009), Ryan et al. (2014)  
C. varanii=C. saurophilum Pavlásek et al. (1995), Koudela & Modry (1998)  Varanus prasinus (Emeriald monitor), Shneider's skinks (Eumeces schneideriLizards Stomach and small intestine 4.4–5.6 (5.0) × 4.2–5.2 (4.7), 4.4–5.6 (5.0) × 4.2–5.2 (5.3) 1.05–1.12 (1.09) Koudela & Modry (1998), Ryan et al. (2014)  
10 C. ducismarci Traversa (2010)  Tortoises Tortoises, turtles, other reptiles NR 4.4–5.4 (5.0) × 4.3–5.3 (4.8) 1.1 ± 0.03 Ježková et al. (2016)  
11 C. testudines Ježková et al. (2016)  Russian tortoises (Testudo horsfieldii, Gray) Tortoises NR 5.8–6.9 (6.4) × 5.3–6.3 (5.9) 1.1 ± 0.05 Ježková et al. (2016)  
Cryptosporidium species reported from birds 
12 C. meleagridis Slavin (1955)  Melleagris gallopova (Turkey) Birds and humans Small intestine 4.5–6.0 (5.0) × 4.2–5.3 (4.4) 1.0–1.3 (1.3) Plutzer & Karanis (2009), Ryan et al. (2014)  
13 C. baileyi Current et al. (1986)  Gallus gallus (Chicken) Birds Bursa, cloacae, trachea 5.6–7.5 (6.4) × 4.8–5.75 (4.8) 1.1–1.4 (1.3) Current et al. (1986), Plutzer & Karanis (2009)  
14 C. galli Pavlásek (1999), Ryan et al. (2003)  Chickens Passeriformes, Phasianidae, Fringillidae, and Icteridae Proventriculus 8.0–8.5 (8.25) × 6.2–6.4 (6.3) 1.30 Ryan et al. (2003)  
15 C. avium Holubová et al. (2016)  Red-crowned parakeets (Cyanoramphus novaezealandiaeBudgerigar, hens Ileum and cecum 5.30–6.90 (6.26) × 4.30–5.5 (4.86) 1.14–1.47 (1.29) Holubová et al. (2016)  
16 C. proventriculi Holubová et al. (2019)  Psittaciformes (Birds) Birds Proventriculus and ventriculus 7.4 × 5.8 NR Holubová et al. (2019)  
Cryptosporidium species reported from mammals 
17 C. muris Tyzzer (1907)  Hause mause (Mus musculusRodents Stomach 8.0–9.0 (8.4) × 5.6–6.4 (6.1), 7.0–9.0 (8.1) × 5.0–6.5 (5.9) 1.25–1.61 (1.38) 1.17–1.7 (1.36) Plutzer & Karanis (2009), Ryan et al. (2014)  
18 C. tyzzery Tyzzer (1912), Ren et al. (2012)  Domestic mice (Mus musculusRodents Jejunum and ileum 4.64 ± 0.05 × 4.19 ± 0.06 1.11 ± 0.02 Ren et al. (2012)  
19 C. proliferans Kváč et al. (2016)  Northeast African mole-rat (Tachyoryctes splendensDonkey, Sciurus eastern grey squirrel, African buffalo, horse Stomach, specifically the glandular part 6.8–8.8 (7.7) × 4.8–6.2 (5.3) 1.48 Kváč et al. (2016)  
20 C. apodemi Čondlová et al. (2018)  Striped field mouse (Apodemus agrariusYellow-necked mice (Apodemus flavicollisIntestine 3.9–4.7 (4.2) × 3.8–4.4 (4.0) 1.0–1.06 (1.03) Čondlová et al. (2018)  
21 C. ditrichi Čondlová et al. (2018)  Yellow-necked mice (Apodemus flavicollisMouse (Mus musculus), human (Homo sapiensSmall intestine – jejunum and ileum 4.5–5.2 (4.7) × 4.0–4.6 (4.2) 1.0–1.2 (1.12) Čondlová et al. (2018)  
22 C. occultus Kváč et al. (2018)  Wild brown rats, mice (Rattus norvegicus), Mongolian gerbils (Meriones unguiculatusRodents Colon 5.20 × 4.94 NR Kváč et al. (2018)  
23 C. alticolis Horčičková et al. (2019)  Common voles (Microtus arvalisVoles Small intestine 5.4 × 4.9 NR Horčičková et al. (2019)  
24 C. macroti Horčičková et al. (2019)  Common voles (Microtus arvalisVoles Large intestine 4.3 × 4.1 NR Horčičková et al. (2019)  
25 C. cuniculus Inman & Takeuchi (1979), Robinson et al. (2010)  European rabbits (Oryctolagus cuniculus) and humans (Homo sapiensRabbits Small intestinal 5.55–6.40 (5.98) × 5.02–5.92 (5.38) 1.1 Robinson et al. (2010)  
26 C. rubeyi Li et al. (2015)  Squirrel (Spermophilus beecheyi, Spermophilus beldingi, Spermophilus lateralisSquirrels NR  4.4–5.0 (4.67) × 4.0–5.0 (4.34) 1.08 Li et al. (2015)  
27 C. felis Iseki (1979)  Felis catis (Cat) Cat Small intestine 6.0–5.0 (5.0) × 5.0–4.5 (4.5) NR Iseki (1979), Plutzer & Karanis (2009), Ryan et al. (2014)  
28 C. canis Fayer et al. (2001)  Canis familiaris (Dog) Dogs Small intestine 4.95 × 4.75 1.05 Fayer et al. (2001), Plutzer & Karanis (2009)  
29 C. wrairi Vetterling et al. (1971)  Cavia porcellus (Guinea pigs) Guinea pigs Small intestine 4.8–5.6 (5.4) × 4.0–5.0 (4.6) 1.17 Plutzer & Karanis (2009), Ryan et al. (2014)  
30 C. homai Zahedi et al. (2017)  Cavia porcellus (Guinea pigs) NR NR NR NR Zahedi et al. (2017)  
31 C. suis Ryan et al. (2004)  Sus scrofa (Pig) Pigs The small and large intestine 4.9–4.4 (4.6) × 4.0–4.3 (4.2) 1.1 Ryan et al. (2004)  
32 C. scrofarum Kváč et al. (2013)  Sus scrofa (Pig) Human, calf, wild boar Duodenum, jejunum, ileum, cecum, colon 4.81–5.96 (5.16) × 4.23–5.29 (4.83) 1.07 ± 0.06 Kváč et al. (2013)  
33 C. parvum Tyzzer (1912)  Bos taurus (Cattle) Ruminants, cattle other livestock, humans Small intestine 4.5–5.4 (4.9) × 4.2–5.2 (4.4) 1.0–1.13 (1.1) Plutzer & Karanis (2009), Ryan et al. (2014)  
34 C. andersoni Lindsay et al. (2000)  Bos taurus (Cattle) Cattle, camel Abomasum 6.0–8.1 (7.4) × 5.0–6.5 (5.5) 1.07–1.50 (1.35) Lindsay et al. (2000)  
35 C. bovis Fayer et al. (2005)  Bos taurus (Cattle) Cattle Small intestine 4.76–5.35 (4.89) × 4.17–4.76 (4.63) 1.06 Fayer et al. (2005)  
36 C. ryanae Fayer et al. (2008)  Bos taurus (Cattle) Cattle NR 2.94–3.68 (3.73) × 2.94–4.41 (3.16) 1.18 Fayer et al. (2008)  
37 C. ubiguitum Fayer et al. (2010)  Bos taurus (Cattle) Ruminants, rodents, carnivores, primates, humans NR 4.71–5.32 (5.04) × 4.33–4.98 (4.66) 1.08 Fayer et al. (2010)  
38 C. pestis Slapeta (2006)  Bos taurus (Cattle) NR NR NR NR Šlapeta (2013)  
39 C. xiaoi Fayer & Santín (2009)  Ovis aries (Sheep) Sheep and goats NR 2.94–4.41 (3.94) × 2.94–4.41 (3.44) 1.15 Fayer & Santín (2009)  
40 C. erinacei Kváč et al. (2014)  European hedgehog (Erinaceus europaeusHedgehogs NR 4.5–5.8 (4.9) × 4.0–4.8 (4.4) 1.02–1.35 (1.13) Kváč et al. (2014)  
41 C. fayeri Ryan et al. (2008)  Red kangaroo (Macropus rufusMarsupials Small intestine 4.5–5.1 (4.9) × 3.8–5.0 (4.3) 1.02–1.18 (1.14) Ryan et al. (2008)  
42 C. macropodum Power & Ryan (2008)  Eastern grey kangaroos (Macropus giganteus). Marsupials Small intestine 5.0–6.0 (5.4) × 4.5–6.0 (4.9) 1.1 Power & Ryan (2008)  
43 C. hominis Morgan-Ryan et al. (2002)  Homo sapiens (Humans) Humans Small intestine 4.4–5.9 (5.2) × 4.4–5.4 (4.86) 1.0–1.09 (1.07) Ryan et al. (2002)  
44 C. viatorum Elwin et al. (2012)  Homo sapiens (Humans) Humans NR NR NR Elwin et al. (2012)  

More than 70 genotypes of Cryptosporidium have been described; 21 species and 4 genotypes out of these have been reported in humans (Feng & Xiao 2017; Holubová et al. 2019). Several Cryptosporidium species are known to be zoonotic with animals as major reservoirs (Feng et al. 2018). Wild and livestock animals have the potential to act as a biological reservoir for harmful protozoan parasites – Cryptosporidium spp. (Xiao & Feng 2008).

Cryptosporidium spp. were first described in mice in 1907 (Tyzzer 1907). Cryptosporidium is part of the Apicomplexa phylum (Phylum: Apicomplexa, Class: Coccidea, Order: Eucoccidiorida, Family: Cryptosporidiidae, Genus: Cryptosporidium) (Fayer & Xiao 2007). Recent taxonomic studies have placed Cryptosporidium as a clad separate from Coccidia. A study on the 18rRNA gene has indicated a closer relation to the gregarines (Apicomplexa, Gregarinia) (Carreno et al. 1999). This would also explain why Cryptosporidium has several features that separate it from other Coccidia: host infection is confined to the apical region of the epithelial cells, the small size of the oocysts, the formation of both thick- and thin-walled oocysts, and the insensitivity to anti-coccidian agents. Further understanding of the relation to the Gregarines is very important for elucidating its ecology and waterborne transmission (Ryan & Xiao 2003; Aldeyarbi & Karanis 2016; Ryan et al. 2016).

Cryptosporidium completes its lifecycle in a single host, and it is ubiquitous in nature. Oocysts can tolerate various environmental conditions and can survive in water and soil for many months because of suitable moisture content and cool temperatures (Smith et al. 2006; King & Monis 2007). They can be transported long distances through air and enter quickly into the water sources because of the oocysts' small size (Vanathy et al. 2017). Cryptosporidium sparked great public health interest after the large human waterborne outbreaks in Milwaukee in 1993 and rapidly was recognized as one of the most serious waterborne pathogens to date (MacKenzie et al. 1994). The outbreaks of cryptosporidiosis have been and continuously reported in several countries (Karanis et al. 2007; Baldursson & Karanis 2011; Efstratiou et al. 2017). Domestic animals, livestock, wildlife, and humans are potential reservoirs that contribute to the contamination of food, surface waters, and the environment by Cryptosporidium spp. Oocysts, thereby transmitting the infection to other hosts via the fecal-oral route (Ahmed & Karanis 2018a, 2018b).

This paper aims to report on the main results of studies on cryptosporidiosis and Cryptosporidium among livestock, wild animals, and birds in Azerbaijan territory and to provide first-hand information about the veterinary and public health aspects of this important pathogen in the Azerbaijan territory for the last 32 years. In total, 13 species of Cryptosporidium from amphibians, reptiles, birds, and mammals have been identified and reported from studies conducted from 1987 to 2019 on structural features of Cryptosporidium oocysts in different regions of the Azerbaijan republic.

We highlighted the occurrence of Cryptosporidium infection in animals particularly in cattle, sheep, goats, pigs, buffaloes, birds, and wild animals in Azerbaijan. A total of 70 studies were used to calculate epidemiological figures.

MATERIAL AND METHODS

Geography

Azerbaijan is situated on the western shore of the Caspian Sea and occupies the north-western and south-eastern parts of the Caucasian Ridge. It borders with the Republic of Dagestan in the north (part of the Russian Federation), in the west with Armenian and the Georgian Republic and in the east the Caspian Sea, and in the south, it borders Iran and Turkey. The territory is divided into five physical-geographical regions: Greater Caucasus, Lesser Caucasus, the Kura-Aras, Lankaran, and the Middle Aras (Figure 1).

Figure 1

Map of Azerbaijan borders.

Figure 1

Map of Azerbaijan borders.

This review has been prepared based on the current literature data. More than 70 publications describing the presence of Cryptosporidium in animals have been published in the last 32 years in Azerbaijan. The language of data collection was English, Russian, and Azeri. The first report of Cryptosporidium was in 1987 (Ismailova & Gaibova 1987). From 1987 to 2019 (32-year period), a total of 9,408 samples from 57 studies on wild animals, birds, and common livestock (defined as cattle, sheep, goats, pigs, horses, and buffaloes) were examined for Cryptosporidium infection, where Cryptosporidium spp. is a widespread pathogen found in many species of domestic animals. Most of the publications (70%) are about Cryptosporidium prevalence in domestic animals. Cryptosporidiosis in livestock has become a significant problem for animal health (both subclinical and clinical) and has resulted in economic losses due to the increase of veterinary services and laboratory costs, increased animal healthcare costs, and a decrease in growth rate with a higher associated mortality in severely infected animals. Stool specimens were randomly collected from 8,668 livestock (pigs, horses, donkeys, goats, sheep, calves, buffalo, zebus, camels, and birds) and 740 wild animals (amphibians, reptiles, rodents, cats, and dogs) (Table 2). The most studied livestock animals were pigs (n = 2,857), cows (n = 2,595), and sheep (n = 1,823) (Table 2).

Table 2

Summarized prevalences of Cryptosporidium reported from animals in Azerbaijan

Hostnamen positive n total%References
Wild animals 
Amphibians 30 87 34.5 Mamedova (2010)  
Reptilia: Ordo: Testudines 58 104 55.8 Gaibova et al. (2017a, 2019), Gaibova & Mamedova (in press)  
Reptilia: Ordo: Squamata 26 114 22.8 
Rodents 112 325 34.5 Gurbanova & Mamedova (2013), Gurbanova (2015), Gaibova et al. (2017a
Cats 17 54 31.5 Gaibova et al. (2017a
Dogs 14 56 25 
Total 257 740 34.7  
Domestic (farm) animals 
Birds 198 729 27.2 Gaibova et al. (2017a), Musaev et al. (1998
Domestic pigs 804 2,857 28.1 Musaev et al. (1996), Haciyeva & Ahmedov (2016
Horse 50 Gaibova et al. (2017a
Donkey 33 
Domestic goat 25 127 19.7 Gaibova & Iskenderova (2012)  
Domestic sheep 623 1,823 34.2 Musaev et al. (1996), Gaibova & Iskenderova (2012, 2014
Cow 779 2,595 30 Musaev et al. (1996), Gaibova & Iskenderova (2012, 2014
Buffalo 135 318 42.5 Gaibova & Iskenderova (2012, 2014
Zebu (Indicine cattle) 14 30 46.7 Gaibova & Iskenderova (2012)  
Bactrian camel 65 182 35.7 Gaibova et al. (2011
Total 2,646 8,668 30.5  
Total 2,903 9,408 30.9  
Hostnamen positive n total%References
Wild animals 
Amphibians 30 87 34.5 Mamedova (2010)  
Reptilia: Ordo: Testudines 58 104 55.8 Gaibova et al. (2017a, 2019), Gaibova & Mamedova (in press)  
Reptilia: Ordo: Squamata 26 114 22.8 
Rodents 112 325 34.5 Gurbanova & Mamedova (2013), Gurbanova (2015), Gaibova et al. (2017a
Cats 17 54 31.5 Gaibova et al. (2017a
Dogs 14 56 25 
Total 257 740 34.7  
Domestic (farm) animals 
Birds 198 729 27.2 Gaibova et al. (2017a), Musaev et al. (1998
Domestic pigs 804 2,857 28.1 Musaev et al. (1996), Haciyeva & Ahmedov (2016
Horse 50 Gaibova et al. (2017a
Donkey 33 
Domestic goat 25 127 19.7 Gaibova & Iskenderova (2012)  
Domestic sheep 623 1,823 34.2 Musaev et al. (1996), Gaibova & Iskenderova (2012, 2014
Cow 779 2,595 30 Musaev et al. (1996), Gaibova & Iskenderova (2012, 2014
Buffalo 135 318 42.5 Gaibova & Iskenderova (2012, 2014
Zebu (Indicine cattle) 14 30 46.7 Gaibova & Iskenderova (2012)  
Bactrian camel 65 182 35.7 Gaibova et al. (2011
Total 2,646 8,668 30.5  
Total 2,903 9,408 30.9  

Fecal samples were collected from wild terrestrial and marine animals, birds, and domestic animals from different natural areas and the urban or rural regions of Azerbaijan in the different seasons of the year.

The diagnosis of cryptosporidiosis relies on the identification of oocysts in fecal samples. The diagnosis is established microscopically. Fine feces smears were fixed with methanol and were stained with carbol-fuchsin and methylene green by the Ziehl–Neelsen staining method or detection of Cryptosporidium oocysts according to the procedure described by Henriksen & Pohlenz (1981). Microscopy is a cheap method but requires a skilled parasitologist and/or related expert and the diagnostic yield is dependent on proper fecal material collection.

Microscopy was the most used technique to diagnose Cryptosporidium infections in animals and human isolates from the reports of the Azerbaijan regions. Cryptosporidium spp. identification was based on conventional criteria, such as oocyst morphology and measurements. These criteria agree with those applied by Fayer et al. (2000) and Morgan-Ryan et al. (2002), who stated that morphometric measurement of oocysts represents the cornerstone of Cryptosporidium taxonomy and is one of the requirements for establishing a new species. Cryptosporidium infections from birds and mammals and attempted cross-transmission studies have been included in this review (Musaev et al. 1997).

RESULTS

Prevalence of Cryptosporidium spp.

A total of 9,408 samples from 57 studies on wild animals, birds, and common livestock (defined as cattle, sheep, goats, pigs, horses, and buffaloes) have been examined for Cryptosporidium infection in the Azerbaijan regions, where 2,903 (30.9%) were positive for Cryptosporidium spp. using microscopy methods. Tables 36 summarize the prevalence and frequency of parasite-positive fecal samples from different groups of animals. All animal groups, with some exceptions, tested positive for Cryptosporidium spp. regarding wild and domestic animals, Cryptosporidium prevalence was higher in wild animals (34.7%) than in farmed animals (30.5%). Fecal samples were collected and tested from 8,668 livestock animals from farms in different regions of Azerbaijan, where 30.5% of them tested positive for Cryptosporidium oocysts. Fecal samples were collected and tested from 740 wild animals captured from different regions of Azerbaijan, from which 34.7% tested positive for Cryptosporidium oocysts (Table 2). The highest prevalence of Cryptosporidium oocysts shedding was observed in feces from testudines (55.8% positive), chickens (50.6% positive), and buffaloes (42.4% positive). Overall, feces from younger (immature) animals were more likely to test positive for Cryptosporidium spp. than feces from adult animals. Furthermore, male animals had a higher Cryptosporidium spp. prevalence than female animals. In the rural and urban areas of Azerbaijan, Cryptosporidium infection was more widespread than in the mountainous areas.

Table 3

Prevalence of Cryptosporidium reported from amphibians in Azerbaijan territory

Host nameGeographic locationn positiven total%References
Amphibians 
Bufo variabilis (European green toad) Absheron 17 36 47.2 Mamedova (2010)  
Lankaran 100 
Bufo verricosissimus (Caucasian toad) Lankaran 16.7 
Hyla savignyi (Lemon-yellow tree frog) Lankaran  
Pelophylax ridibundus (Euroasian marsh frog) Lankaran 28 32.1 
Shabran  
Gobustan  
Gabala  
Total  30 87 34.5 
Host nameGeographic locationn positiven total%References
Amphibians 
Bufo variabilis (European green toad) Absheron 17 36 47.2 Mamedova (2010)  
Lankaran 100 
Bufo verricosissimus (Caucasian toad) Lankaran 16.7 
Hyla savignyi (Lemon-yellow tree frog) Lankaran  
Pelophylax ridibundus (Euroasian marsh frog) Lankaran 28 32.1 
Shabran  
Gobustan  
Gabala  
Total  30 87 34.5 
Table 4

Prevalence of Cryptosporidium reported in reptilians from Azerbaijan territory

Host nameGeographic locationn positiven total%References
Reptilians 
Ordo: Testudines 
Emys orbicularis (European pond turtle) Absheron 23 24 95.8 Gaibova et al. (2019)  
Shabran 16 
Mauremys caspica (East Caspian turtle) Lankaran 100 Gaibova & Mamedova (in press)  
Absheron 16 16 100 Gaibova et al. (2019)  
Testudo graeca (Greek tortoise) Absheron 23 8.7 Gaibova & Mamedova (in press)  
Gakh district 75 
Absheron 100 Gaibova et al. (2019)  
Balakan, Zagatala districts 14 50.0 Gaibova et al. (2017a)  
Total (Testudines)  58 104 55.8  
Ordo: Squamata 
Tenuidactylus caspius (Caspian Bent-toed gecko) Absheron 19 21.1 Gaibova & Mamedova (in press)  
Gobustan  
Paralaudakia caucasia (Caucasian agama) Gobustan 11 68 16.2 
Eremias arguta (Steppe-runner) Shirvan 50 
Eirenis collaris (Collared dwarf racer) Gobustan 33.3 
Hemоrrhois ravergieri (Spotted whip snake) Gobustan district 50 
Natrix tessellata (Dice snake) Absheron 11 11.5 
Macrovipera lebetina (Levantine viper) Balakan, Zagatala districts 25.0 Gaibova et al. (2017a)  
Total (Squamata)  26 114 22.8  
Total  84 218 38.5  
Host nameGeographic locationn positiven total%References
Reptilians 
Ordo: Testudines 
Emys orbicularis (European pond turtle) Absheron 23 24 95.8 Gaibova et al. (2019)  
Shabran 16 
Mauremys caspica (East Caspian turtle) Lankaran 100 Gaibova & Mamedova (in press)  
Absheron 16 16 100 Gaibova et al. (2019)  
Testudo graeca (Greek tortoise) Absheron 23 8.7 Gaibova & Mamedova (in press)  
Gakh district 75 
Absheron 100 Gaibova et al. (2019)  
Balakan, Zagatala districts 14 50.0 Gaibova et al. (2017a)  
Total (Testudines)  58 104 55.8  
Ordo: Squamata 
Tenuidactylus caspius (Caspian Bent-toed gecko) Absheron 19 21.1 Gaibova & Mamedova (in press)  
Gobustan  
Paralaudakia caucasia (Caucasian agama) Gobustan 11 68 16.2 
Eremias arguta (Steppe-runner) Shirvan 50 
Eirenis collaris (Collared dwarf racer) Gobustan 33.3 
Hemоrrhois ravergieri (Spotted whip snake) Gobustan district 50 
Natrix tessellata (Dice snake) Absheron 11 11.5 
Macrovipera lebetina (Levantine viper) Balakan, Zagatala districts 25.0 Gaibova et al. (2017a)  
Total (Squamata)  26 114 22.8  
Total  84 218 38.5  
Table 5

Prevalence of Cryptosporidium reported in birds from Azerbaijan territory

HostnameGeographic locationn positiven total%References
Gallus domesticus (Chickens) Poultry farms in Absheron 135 269 50.6 Musaev et al. (1998)  
Phasianus colchicus (Pheasants) Poultry farms in Absheron 16 203 7.9 
Pavo cristatus (Peacocks) Poultry farms in Absheron 62 12.9 
Coturnix coturnix (Quails) Poultry farms in Absheron 26 120 21.7 
Columba livia Gm. (Rock dove) Balakan, Gakh, Zagatala districts 60 13.3 Gaibova et al. (2017a)  
Anser anser (Grey goose) Balakan, Gakh, Zagatala districts 43.0 
Anser Penelope (Grey duck) Balakan, Gakh, Zagatala districts 25.0 
Total  198 729 27.2 
HostnameGeographic locationn positiven total%References
Gallus domesticus (Chickens) Poultry farms in Absheron 135 269 50.6 Musaev et al. (1998)  
Phasianus colchicus (Pheasants) Poultry farms in Absheron 16 203 7.9 
Pavo cristatus (Peacocks) Poultry farms in Absheron 62 12.9 
Coturnix coturnix (Quails) Poultry farms in Absheron 26 120 21.7 
Columba livia Gm. (Rock dove) Balakan, Gakh, Zagatala districts 60 13.3 Gaibova et al. (2017a)  
Anser anser (Grey goose) Balakan, Gakh, Zagatala districts 43.0 
Anser Penelope (Grey duck) Balakan, Gakh, Zagatala districts 25.0 
Total  198 729 27.2 
Table 6

Prevalence of Cryptosporidium reported in mammals from Azerbaijan territories

Host nameGeographic locationn positiven total%References
Rattus norvegicus (Brown rat) Gakh 11 72.7 Gurbanova Mamedova (2013)  
Absheron, Gobustan 23 54 42.6 Gurbanova (2015)  
Balakan, Zagatala districts 44.4 Gaibova et al. (2017a
Mus musculus (Hause mouse) Absheron, Gobustan 26 107 24.5 Gurbanova (2015)  
Balakan, Gakh, Zagatala districts 13 21 62.0 Gaibova et al. (2017a
Meriones libycus (Libyan jird) Absheron, Gobustan 38 123 30.9 Gurbanova (2015)  
Total  112 325 34.5  
Canis lupus familiaris (Dog) Balakan, Gakh, Zagatala districts 14 56 25 Gaibova et al. (2017a
Félis silvéstris cátus (Cat) Balakan, Gakh, Zagatala districts 17 54 31.5 
Total  31 110 28.2  
Sus scrofa domesticus (Domestic pig) Pig farms in Absheron 201 1,078 18.6 Musaev et al. (1996)  
Pig farms in Absheron 339 874 39.0 Haciyeva Ahmadov (2016)  
Pig farms in Shamakhi 94 393 24.0 
Pig farms in Khudat 83 195 42.5 
Pig farms in Ismayilli 43 220 19.5 
Pig farms in Salyan 44 97 45.3 
Total  804 2,857 28.1  
Equus ferus caballus (Horse) Balakan, Qakh, Zaqatala districts  Gaibova et al. (2017a)  
Equus africanus asinus (Donkey) Balakan, Qakh, Zaqatala districts  
Total  3 7 42.9  
Capra aegagrus hircus (Domestic goat) Absheron, Shabran, Samukh districts 14 57 24.5 Gaibova Iskenderova (2012)  
Ganja, Goygol district 35 17.1 
Dashkasan district 35 14.3 
Total  25 127 19.7  
Ovis aries (Domestic sheep) Farms in Absheron 139 612 22.7 Musaev et al. (1996)  
Absheron, Shabran, Samux 16 220 7.3 Gaibova Iskenderova (2012)  
Ganca, Goygol district 35 58 60.3 
Dashkasan district 30 57 52.6 
Gobustan district 48 143 33.6 
Balakan, Gakh, Zagatala districts 355 733 48.4 Gaibova Iskenderova (2014)  
Total  623 1,823 34.2  
Bos taurus (Cow) Farms in Absheron 366 1,736 21.1 Musaev et al. (1996)  
Absheron, Shabran, Samukh 25 105 24.0 Gaibova Iskenderova (2012)  
Ganja, Goygol district 10 56 17.9 
Dashkasan district 10 55 18.2 
Gobustan district 93 179 51.9 Gaibova Iskenderova (2014)  
Balakan, Gakh, Zagatala districts 275 464 59.3 
Total  779 2,595 30.02  
Bubalus bubalis (Buffalo) Absheron, Shabran Samukh  Gaibova Iskenderova (2012)  
Ganja, Goygol district 15 70 21.4 
Dashkasan district 15 75 20.0 
Balakan, Gakh, Zagatala districts 105 170 61.8 Gaibova Iskenderova (2014)  
Total  135 318 42.5  
Bos taurus indicus Zebu (Indicine cattle) Absheron, Shabran, Samukh 15 46.7 Gaibova Iskenderova (2012)  
Dashkasan district 15 46.7 
Total  14 30 46.7  
Camelus bactrianus (Bactrian camel) Farms in Salyan district 65 182 35.7 Gaibova et al. (2011)  
Total  2,591 8,374 30.9  
Host nameGeographic locationn positiven total%References
Rattus norvegicus (Brown rat) Gakh 11 72.7 Gurbanova Mamedova (2013)  
Absheron, Gobustan 23 54 42.6 Gurbanova (2015)  
Balakan, Zagatala districts 44.4 Gaibova et al. (2017a
Mus musculus (Hause mouse) Absheron, Gobustan 26 107 24.5 Gurbanova (2015)  
Balakan, Gakh, Zagatala districts 13 21 62.0 Gaibova et al. (2017a
Meriones libycus (Libyan jird) Absheron, Gobustan 38 123 30.9 Gurbanova (2015)  
Total  112 325 34.5  
Canis lupus familiaris (Dog) Balakan, Gakh, Zagatala districts 14 56 25 Gaibova et al. (2017a
Félis silvéstris cátus (Cat) Balakan, Gakh, Zagatala districts 17 54 31.5 
Total  31 110 28.2  
Sus scrofa domesticus (Domestic pig) Pig farms in Absheron 201 1,078 18.6 Musaev et al. (1996)  
Pig farms in Absheron 339 874 39.0 Haciyeva Ahmadov (2016)  
Pig farms in Shamakhi 94 393 24.0 
Pig farms in Khudat 83 195 42.5 
Pig farms in Ismayilli 43 220 19.5 
Pig farms in Salyan 44 97 45.3 
Total  804 2,857 28.1  
Equus ferus caballus (Horse) Balakan, Qakh, Zaqatala districts  Gaibova et al. (2017a)  
Equus africanus asinus (Donkey) Balakan, Qakh, Zaqatala districts  
Total  3 7 42.9  
Capra aegagrus hircus (Domestic goat) Absheron, Shabran, Samukh districts 14 57 24.5 Gaibova Iskenderova (2012)  
Ganja, Goygol district 35 17.1 
Dashkasan district 35 14.3 
Total  25 127 19.7  
Ovis aries (Domestic sheep) Farms in Absheron 139 612 22.7 Musaev et al. (1996)  
Absheron, Shabran, Samux 16 220 7.3 Gaibova Iskenderova (2012)  
Ganca, Goygol district 35 58 60.3 
Dashkasan district 30 57 52.6 
Gobustan district 48 143 33.6 
Balakan, Gakh, Zagatala districts 355 733 48.4 Gaibova Iskenderova (2014)  
Total  623 1,823 34.2  
Bos taurus (Cow) Farms in Absheron 366 1,736 21.1 Musaev et al. (1996)  
Absheron, Shabran, Samukh 25 105 24.0 Gaibova Iskenderova (2012)  
Ganja, Goygol district 10 56 17.9 
Dashkasan district 10 55 18.2 
Gobustan district 93 179 51.9 Gaibova Iskenderova (2014)  
Balakan, Gakh, Zagatala districts 275 464 59.3 
Total  779 2,595 30.02  
Bubalus bubalis (Buffalo) Absheron, Shabran Samukh  Gaibova Iskenderova (2012)  
Ganja, Goygol district 15 70 21.4 
Dashkasan district 15 75 20.0 
Balakan, Gakh, Zagatala districts 105 170 61.8 Gaibova Iskenderova (2014)  
Total  135 318 42.5  
Bos taurus indicus Zebu (Indicine cattle) Absheron, Shabran, Samukh 15 46.7 Gaibova Iskenderova (2012)  
Dashkasan district 15 46.7 
Total  14 30 46.7  
Camelus bactrianus (Bactrian camel) Farms in Salyan district 65 182 35.7 Gaibova et al. (2011)  
Total  2,591 8,374 30.9  

Cryptosporidium infection in amphibians and reptilians

Relatively little is known about Cryptosporidium in amphibians, and currently, the only accepted species is Cryptosporidium fragile, which was described from the stomach of naturally infected black-spined toads (Duttaphrynus melanostictus) from the Malay peninsula in Southeast Asia (Jirku et al. 2008; Table 1).

The first report of Cryptosporidium oocysts in amphibians from Azerbaijan was in 2010. Cryptosporidium oocysts were found in the feces of all examined amphibian species except for European tree frogs (Table 3). We found that the morphometric characteristics of Cryptosporidium oocysts from Bufo verrucomsissimus are similar to those of the only valid amphibian Cryptosporidium species, C. fragile. These oocysts had an average size of 6.31 ± 0.01 × 5.01 ± 0.01 μm. In general, all the oocysts had an elongated oval shape, with a length/width ratio of 1.24. The prevalence of Cryptosporidium in the Absheron peninsula and Lankaran lowland was higher than the mountainous regions (Mamedova 2010).

The first report of Cryptosporidium in tortoise described oocyst detection using microscopy in the feces of an Indian star tortoise, Geochelone elegans (Schoepff 1795), which is kept in a zoo in the USA (Heuschele et al. 1986). Cryptosporidium ducismarci has been reported in several species of tortoises, snakes, and lizards (Traversa 2010). C. testudinis is a parasite of the tortoise, and its oocysts are significantly larger than those of C. ducismarci, allowing these two species to be distinguished microscopically (Ježková et al. 2016).

In the years from 2008 to 2019, a total of 104 tortoise and turtles (3 species: Emys orbicularis (European pond turtle), Mauremys caspica (East Caspian turtle), and Testudo graeca (Greek tortoise)) were examined for the presence of Cryptosporidium and other gastrointestinal parasites from Azerbaijan (Table 4).

Fifty-eight of them (55.8%) were infected with Cryptosporidium oocysts. The Cryptosporidium oocysts from Testudo graeca specimens caught in the territory of Absheron peninsula and in the territory Gakh district were morphologically compared. Oocysts from the territory of Absheron peninsula measured 5.5 ± 0.1 × 4.9 ± 0.01 μm and had a length/width index of 1.12 ± 0.03, and the oocysts obtained from the territory Gakh district were similar in size and measured 5.2 ± 0.4 × 4.02 ± 0.34 μm, with an index of 1.1 ± 0.03. The oocysts isolated from the Testudo graeca specimens were morphologically similar to C. ducismarci that is described in the literature. It was the first time that C. ducismarci was found in a Greek tortoise (T. graeca). Reptiles caught in the territory of the Absheron peninsula showed a higher prevalence (100%) than reptiles caught in the mountainous territory (50%) (Gaibova & Mamedova in press).

Cryptosporidium serpentis (Levine 1980) and C. varanii (syn. Cryptosporidium saurophilum) are the only valid species associated with reptile reservoirs (Ordo: Squamata) (Pavlásek et al. 1995; Pavlasek & Ryan 2008; Plutzer & Karanis 2009; Table 1).

A total of 160 specimens belonging to 18 species of ordo Squamata were examined for Cryptosporidium (Gaibova & Mamedova in press). Cryptosporidium oocysts were found in the feces of 114 reptiles from 7 species (Table 4).

Cryptosporidium oocysts that infected the Caucasian agama (Paralaudakia caucasia) (oocysts were 6.4 ± 0.2 by 5.6 ± 0.1 μm, a length/width index of 1.2 ± 0.02) and the Steppe-runner (Eremias arguta) (oocysts were 6.4 ± 0.2 by 4.7 ± 0.1 μm, a length/width index of 1.4 ± 0.1) had morphological characteristics related to C. serpentis. Oocysts from the feces of a naturally infected Spotted whip snake (Hemоrrhois ravergieri) and Dice snake (Natrix tessellate) measured 4.7 ± 0.1 × 4.4 ± 0.1 μm, with a length/width ratio of 1.07 ± 0.02 and 4.9 ± 0.1 × 4.8 ± 0.2 μm, and a length/width ratio of 1.07 ± 0.02, respectively. The authors reported that these oocysts were morphologically indistinguishable from those of C. varanii. For the first time, the Caucasian agama (Paralaudakia caucasia) and Steppe-runner (Eremias arguta) have been identified as the host of C. serpentis; and the Spotted whip snake (Hemоrrhois ravergieri) and Dice snake (Natrix tessellate) for C. varanii. Reptiles caught from the territory of Absheron and Gobustan showed a higher prevalence of Cryptosporidium than other Azerbaijan regions (Gaibova & Mamedova in press).

Cryptosporidium infection in birds

Cryptosporidiosis is one of the main protozoan infections among birds. Cryptosporidium species have been reported in more than 30 avian species worldwide (Sreter & Varga 2000). The first description of Cryptosporidium infection among birds (chicken) was reported by Tyzzer (1929). In 1955, a new species namely C. melagridis was reported to cause illness and death in young turkeys (Slavin 1955). Later, cryptosporidiosis was diagnosed among domestic geese (Anser anser) (Proctor & Kemp 1974) and broiler chickens (Fletcher et al. 1975). Current et al. (1986) described the biological cycle of Cryptosporidium in domestic chickens and named its species, C. baileyi. The third valid species of this parasite in birds, C. galli, was described by Pavlásek (1999) from the proventriculi of chickens and later was revised by Ryan et al. (2003). To date, five species of Cryptosporidium (C.meleagridis, C. baileyi, C. galli, C. avium, and C. proventriculi) have been described in birds (Table 1).

Between 1987 and 2019, a total of 729 fecal samples from birds were collected from different regions in Azerbaijan. According to the microscopy results using Ziehl–Neelsen staining, Cryptosporidium oocysts were present in 27.2% of the samples. The first report of Cryptosporidium in birds from Azerbaijan was in 1998. A total of 654 bird fecal samples from four species were examined for the Cryptosporidium spp. infection during the 9-year study (1989–1998) from farms in the Absheron peninsula, where 185 of them (28.3%) were infected by Cryptosporidium oocysts. The extent of Cryptosporidium oocysts infection in chickens, pheasants, peacocks, and quails were 50.6% (135/269), 7.9% (16/203), 12.9% (8/62), and 21.7% (26/120), respectively (Musaev et al. 1998). The highest prevalence of Cryptosporidium was in chickens (50.6%) (Table 5).

Oocysts from the feces of chickens measured 5.3 × 4.6 μm and had a length/width ratio of 1.15, pheasants measured 4.4 × 3.9 μm and had a length/width ratio of 1.13, peacocks measured 4.7 × 4.15 μm and had a length/width ratio of 1.3, and quails measured 5.14 × 4.8 μm and had a length/width ratio of 1.07. The two Cryptosporidium species (C. meleagridis and C. baileyi) that were detected in bird fecal smears from the study areas in Azerbaijan were morphologically similar to the oocysts from the same bird species that were detected in previous studies (Zha & Jiang 1994; Fujino 1996; Ryan et al. 2003).

Cryptosporidium infection in mammals

Mammals represent the largest group of animals known to be infected with Cryptosporidium spp. Cryptosporidium infections have been reported in at least 155 mammalian species (O'Donogue 1995; Fayer et al. 1997; Fayer & Xiao 2007). Wild animals seem to be involved in the epidemiology of most zoonoses and serve as major reservoirs for the transmission to domestic animals and humans (Kruse et al. 2004). C. muris, C. tyzzeri, C. proliferans, C. apodemi, C. ditrichi, C. occultus, C. alticolis, C. macroti, C. ubiquitum, and C. tyzzeri are known parasites of rodents (Table 1).

Three-hundred and twenty-five rodents from three species from the Azerbaijan territories were examined for Cryptosporidium oocysts and 112 (34.5%) of them were infected (Table 6). Oocysts appeared as round or ellipsoid formations. Oval oocysts measuring 5.06 × 4.0 μm, whereas ellipsoidal oocysts measured 7.50 × 5.50 μm. In Azerbaijan, three species of Cryptosporidium, such as C. muris, C. parvum, and C. ubiquitum, from rodents have been reported (Gurbanova & Mamedova 2013; Gurbanova 2015; Gaibova et al. 2017b).

Cryptosporidium spp. were first reported in cats in Japan (Iseki 1979), later it was called C. felis. The first evidence of cryptosporidiosis in dogs was reported by Tzipory & Campbell (1981), which was labeled as C. canis. After the examination of 110 dogs and cats caught from the mountainous regions in the Azerbaijan, Cryptosporidium oocysts were detected in 25% of dog and 31.5% of cat specimens (Table 6).

Cryptosporidium is a parasite responsible for widespread disease in livestock. The great majority of infections have been reported in domestic animals of economic importance, such as cattle, pigs, and sheep. Studies worldwide suggest that cattle are infected with four major Cryptosporidium species: C. parvum, C. bovis, C. andersoni, and C. ryanae (Xiao & Feng 2008; Xiao 2010; Ryan et al. 2014).

At least 8 Cryptosporidium species have been identified in sheep feces, including C. parvum, C. hominis, C. andersoni, C. suis, C. xiaoi, C. fayeri, C. ubiquitum, and C. scrofarum. C. xiaoi, C. ubiquitum, and C. parvum that had the highest prevalence. C. parvum, C. hominis, C. ubiquitum, and C. xiaoi have also been identified in goats. The main Cryptosporidium species identified in pigs worldwide are C. suis and C. scrofarum, although C. muris, C. tyzzeri, and C. parvum have also been reported in pigs (Ryan et al. 2014; Table 1).

The prevalence of Cryptosporidium in cattle, sheep, goats, buffaloes, and pigs has been studied in Azerbaijan. The first report was published in 1996 (Musaev et al. 1996). During a 32-year period from 1987 to 2019, a total of 7,750 (2,595 calves, 318 buffalo, 30 zebus, 1,823 sheep, 127 goats, and 2,857 pigs) stool samples were examined for Cryptosporidium (Table 4). Oocysts from the feces of a naturally infected large and young cattle and buffalo measured 5.0 × 4.7 (4.4–5.6 × 4.2–5.2) μm, with a length/width ratio of 1.05. We presented the data on relevant Cryptosporidium oocysts in feces from cattle, pigs, and sheep of different ages and the results of experimentally infected laboratory animals (rats, mice, rabbits, and coypus) with oocysts as well. Younger domestic animals showed a higher prevalence of oocyst shedding than older domestic animals. The Coccidia, from the genera Cryptosporidium, parasitize the older and younger cattle and buffalo in the Azerbaijan farm economies that were studied from 2005 to 2008, which were situated at different heights above the sea level (Gaibova & Iskenderova 2012). In the farm communities from the vertical belts, lowlands, foothills, and mountains, all reported that the younger cattle suffered higher consequences of Cryptosporidium infection than larger cattle and buffalo. The prevalence of Cryptosporidium in sheep was higher in the mountainous regions than in cows, goats, or buffalo that were raised in the lowland areas. Three species of Cryptosporidium were found in older and younger cattle and buffalo in Azerbaijan: C. andersoni, C. bovis, and C. hominis (Gaibova et al. 2017b).

In total, 182 Bactrian camels from Azerbaijan were investigated for Cryptosporidium, whereas 65/182 (35.7%) of them were infected with Cryptosporidium oocysts (Table 6), and younger camels showed a higher prevalence than the older camels. The highest prevalence of infection was recorded during the autumn season. Oocysts appeared either as round or oval formations, with a diameter 3.34–5.01 μm, nearly spherical (a length/width ratio of 1.02 ± 0.003) with a measurement of 5.0 ± 0.03 × 4.92 ± 0.03 μm, or even larger with a measurement of 7.4 ± 0.23 × 6.9 ± 0.17 μm, with a length/width ratio of 1.05 ± 0.003. Two species of Cryptosporidium, namely C. muris and C. andersoni, were noted in the camel study (Gaibova et al. 2011).

In the years 2009–2015, a total of 2,857 pigs were examined for the presence of Cryptosporidium, whereas 804 (28.1%) of them were infected with Cryptosporidium oocysts (Table 6). The extent of invasion with Cryptosporidium was higher in the lowland areas of the Absheron peninsula (39%) and in the Salyan region (45.3%). In the foothill area, Khudat had a 42.5% prevalence, and the mountains of Shamakhi 24% and Ismayilli 19.5%. Most of the detected Cryptosporidium oocysts were in the medium size range of 4.7–4.0 μm. These authors also obtained larger oocysts that measured 7.5 × 7.0 μm in the study. Two species of Cryptosporidium were found in pigs from Azerbaijan, C. muris and C. suis (Haciyeva & Ahmadov 2016).

Cryptosporidium infections in small ruminants may be a source for cryptosporidiosis in humans. In particular, sheep and goats are the known reservoirs of Cryptosporidium in cases of human infections (Koinari et al. 2014). Cryptosporidium outbreaks in school children have been associated with contact with lamb/goat kids as reported in the literature (Lange et al. 2014).

The diagnosis of cryptosporidiosis relies on the identification of oocysts in fecal samples released by the infected host. Stool specimens were processed using the modified acid-fast staining method (Ziehl–Neelsen (mZN)) and microscopically examined for Cryptosporidium oocysts. Thirteen species of Cryptosporidium (C. fragile, C. ducismarci, C. serpentis, C. varanii, C. baileyi, C. meleagridis, C. muris, C. parvum, C. ubiquitum, C. andersoni, C. bovis, C. hominis, and C. suis) have been reported from amphibians, reptiles, birds, and mammals that were identified from the studies conducted from 1987 to 2019 on the structural features of Cryptosporidium oocysts in Azerbaijan territory (Table 7). These species of Cryptosporidium were identified by microscopy and mZN staining from fecal samples of animal specimens collected in the studies. The prevalence of Cryptosporidium in Absheron peninsula and Lankaran lowland was higher than in the mountainous regions from these animals.

Table 7

Cryptosporidium species reported from animals (wild, domestic, birds, reptiles, and amphibians) in Azerbaijan territory

Cryptosporidium speciesHostsDimension (μm)L/W (Length/Width)
Cryptosporidium fragile Bufo verricosissimus – Caucasian toad 6.31 ± 0.01 × 5.01 ± 0.01 1.24 
Cryptosporidium ducismarci Testudo graeca – Greek tortoise 5.5 ± 0.1 × 4.9 ± 0.01, 5.2 ± 0.4 × 4.02 ± 0.34 1.12 ± 0.03, 1.1 ± 0.03. 
Cryptosporidium serpentis Paralaudakia caucasia – Caucasian agama 6.4 ± 0.2 × 5.6 ± 0.1 1.2 ± 0.02 
Eremias arguta – Steppe-runner 6.4 ± 0.2 × 4.7 ± 0.1 1.4 ± 0.1 
Cryptosporidium varanii Hemоrrhois ravergieri – Spotted whip snake 4.7 ± 0.1 × 4.4 ± 0.1 1.07 ± 0.02 
Natrix tessellate – Dice snake 4.9 ± 0.1 × 4.8 ± 0.2 1.07 ± 0.02 
Cryptosporidium baileyi Gallus domesticus (Chickens) 5.3 × 4.6 1.15 
Cryptosporidium meleagridis Phasianus colchicus (Pheasants) 4.4 × 3.9 1.13 
Pavo cristatus (Peacocks) 4.7 × 4.15 1.3 
Coturnix coturnix (Quails) 5.14 × 4.8 1.07 
Cryptosporidium muris Mus musculus – Hause mause 7.73–7.91 × 5.50–7.73 1.29 
Rattus norvegicus – Brown rat, 7.53–7.85 × 6.40–7.85 1.04–1.17 
Meriones libycus – Libyan jird 7.66–7.94 × 5.50–7.73 1.38–1.41 
Calves 8.35 × 6.68 1.0 
Pigs 7.5 × 7.05 1.02 
Cryptosporidium parvum Mus musculus – Hause mause 5.06 × 4.05 1.0 
Rattus norvegicus – Brown rat 5.01 × 3.89 1.0 
Camel 5.0 ± 0.03 × 4.92 ± 0.03 1.02 ± 0.003 
Calves 5.01 × 4.2 1.0 
Sheep 5.85 × 5.01 1.0 
Human 5.01 × 4.2 1.0 
Cryptosporidium ubiquitum Mus musculus – Hause mause, Rattus norvegicus – Brown rat, Meriones libycus – Libyan jird 5.01 × 4.35 1.08 
Cryptosporidium andersoni Camel 7.4 ± 0.23 × 6.9 ± 0.17 1.05 ± 0.003 
Sheep, goat 6.3 ± 0.07 × 6.08 ± 0.08 1.03 
Calves, buffalo 6.7–5.85 × 6.7–5.01 1.0–1.2 
Cryptosporidium bovis Large and small cattle 5.0 × 4.7 (4.4–5.6 × 4.2–5.2) 1.05 
Cryptosporidium hominis Calves, buffalo, sheep, human 4.35 ± 0.16 × 3.9 ± 0.14 (5.8–5.01 × 4.2–3.34) 1.1 
Cryptosporidium suis Pigs 4.7 × 4.0 1.03 
Cryptosporidium speciesHostsDimension (μm)L/W (Length/Width)
Cryptosporidium fragile Bufo verricosissimus – Caucasian toad 6.31 ± 0.01 × 5.01 ± 0.01 1.24 
Cryptosporidium ducismarci Testudo graeca – Greek tortoise 5.5 ± 0.1 × 4.9 ± 0.01, 5.2 ± 0.4 × 4.02 ± 0.34 1.12 ± 0.03, 1.1 ± 0.03. 
Cryptosporidium serpentis Paralaudakia caucasia – Caucasian agama 6.4 ± 0.2 × 5.6 ± 0.1 1.2 ± 0.02 
Eremias arguta – Steppe-runner 6.4 ± 0.2 × 4.7 ± 0.1 1.4 ± 0.1 
Cryptosporidium varanii Hemоrrhois ravergieri – Spotted whip snake 4.7 ± 0.1 × 4.4 ± 0.1 1.07 ± 0.02 
Natrix tessellate – Dice snake 4.9 ± 0.1 × 4.8 ± 0.2 1.07 ± 0.02 
Cryptosporidium baileyi Gallus domesticus (Chickens) 5.3 × 4.6 1.15 
Cryptosporidium meleagridis Phasianus colchicus (Pheasants) 4.4 × 3.9 1.13 
Pavo cristatus (Peacocks) 4.7 × 4.15 1.3 
Coturnix coturnix (Quails) 5.14 × 4.8 1.07 
Cryptosporidium muris Mus musculus – Hause mause 7.73–7.91 × 5.50–7.73 1.29 
Rattus norvegicus – Brown rat, 7.53–7.85 × 6.40–7.85 1.04–1.17 
Meriones libycus – Libyan jird 7.66–7.94 × 5.50–7.73 1.38–1.41 
Calves 8.35 × 6.68 1.0 
Pigs 7.5 × 7.05 1.02 
Cryptosporidium parvum Mus musculus – Hause mause 5.06 × 4.05 1.0 
Rattus norvegicus – Brown rat 5.01 × 3.89 1.0 
Camel 5.0 ± 0.03 × 4.92 ± 0.03 1.02 ± 0.003 
Calves 5.01 × 4.2 1.0 
Sheep 5.85 × 5.01 1.0 
Human 5.01 × 4.2 1.0 
Cryptosporidium ubiquitum Mus musculus – Hause mause, Rattus norvegicus – Brown rat, Meriones libycus – Libyan jird 5.01 × 4.35 1.08 
Cryptosporidium andersoni Camel 7.4 ± 0.23 × 6.9 ± 0.17 1.05 ± 0.003 
Sheep, goat 6.3 ± 0.07 × 6.08 ± 0.08 1.03 
Calves, buffalo 6.7–5.85 × 6.7–5.01 1.0–1.2 
Cryptosporidium bovis Large and small cattle 5.0 × 4.7 (4.4–5.6 × 4.2–5.2) 1.05 
Cryptosporidium hominis Calves, buffalo, sheep, human 4.35 ± 0.16 × 3.9 ± 0.14 (5.8–5.01 × 4.2–3.34) 1.1 
Cryptosporidium suis Pigs 4.7 × 4.0 1.03 

These investigations confirmed that Cryptosporidium spp. are common parasites of wild and domestic animals, birds, reptiles, and amphibians in Azerbaijan. The prevalence of Cryptosporidium infection was higher in the rural than the urban areas of Azerbaijan. Additional investigations are in progress to further evaluate and estimate the widespread prevalence and distribution of this pathogen throughout Azerbaijan. There is a significant cryptosporidiosis risk for animals and humans from contaminated fecal material in the water and food supply. A unified public health policy needs to be implemented to protect the susceptible human and animal populations.

CONCLUSION

The present review has shown that there is a high prevalence of Cryptosporidium spp. (more than 30%) in the areas studied in Azerbaijan. The studies of Cryptosporidium infection in animals and livestock from different regions of Azerbaijan have revealed the following distribution pattern: the highest prevalence of infection was recorded in the lowland areas and the lowest prevalence was recorded in the mountainous regions. The highest rate of infection with Cryptosporidium was found in reptiles and amphibians and other terrestrial animals from the Absheron peninsula and Gobustan reserve. The Absheron peninsula is the most urbanized territory of the Republic of Azerbaijan, where Cryptosporidium transmission from reptile and amphibian reservoirs could have a negative impact on human and animal health.

The review has shown that Cryptosporidium spp. is a common parasite of animals in Azerbaijan. Herein, 13 species of Cryptosporidium from amphibians, reptiles, birds, and mammals have been identified based on the structural features of Cryptosporidium oocysts from this country.

Cryptosporidium species have been determined based on a comparative analysis of morphometric parameters of oocysts found in stool specimens that are consistent with previously described species of Coccidia. The morphological features of Cryptosporidium oocysts have been essential for Cryptosporidium species identification. However, further lifecycle studies and DNA analyses are recommended to complement the morphometric characteristics of Cryptosporidium found in Azerbaijan. These studies will be key to the understanding of Cryptosporidium epidemiology and transmission in domestic and wild animals, natural environment, and humans living in Azerbaijan.

ACKNOWLEDGEMENTS

We acknowledge Chad Schou, University of Nicosia Medical School, Cyprus, for the time and effort devoted to improving the linguistic quality of this review.

DATA AVAILABILITY STATEMENT

All relevant data are included in the paper or its Supplementary Information.

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